Can skilled readers perform a second task in parallel? A functional connectivity MRI study

When asked to search for a target letter while reading, the patterns with which people miss the target letter reveal information about the process of reading itself. Questions remain as to whether this paradigm reflects normal reading processes however. We used a novel continuous-performance neuroimaging paradigm to address this question. In separate scanning runs, subjects either read alone, read while searching for a target letter, or searched non-words continuously. Functional connectivity analysis recovered the full extent of brain areas identified for reading in a localizer scan, with no differences between reading alone and the dual task condition. Differences were found, however, between both reading conditions and the nonword search condition. These results demonstrate that in skilled readers brain activation associated with reading is unaffected by a concurrent letter-search task. They further demonstrate the utility of a naturalistic, continuous-performance paradigm for studying the neural basis of language processing.

[1]  A. Mechelli,et al.  Reading and reading disturbance , 2005, Current Opinion in Neurobiology.

[2]  Alice F. Healy,et al.  The Unitization Effect in Reading Chinese and English Text , 2002 .

[3]  Elliot B. Sloane Rapid serial visual presentation (RSVP) for professional tasks : a trial study of an accelerated reading display for citation relevance judgements by domain experts , 1999 .

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

[5]  M. Masson Conceptual processing of text during skimming and rapid sequential reading , 1983, Memory & cognition.

[6]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[7]  M. Ullman A neurocognitive perspective on language: The declarative/procedural model , 2001, Nature Reviews Neuroscience.

[8]  Stephen M. Smith,et al.  Probabilistic independent component analysis for functional magnetic resonance imaging , 2004, IEEE Transactions on Medical Imaging.

[9]  J. Don Read Detection of Fs in a single statement: The role of phonetic recoding , 1983, Memory & cognition.

[10]  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.

[11]  Daniel B. Willingham,et al.  On the development of procedural knowledge. , 1989, Journal of experimental psychology. Learning, memory, and cognition.

[12]  A. Friederici,et al.  Auditory Language Comprehension: An Event-Related fMRI Study on the Processing of Syntactic and Lexical Information , 2000, Brain and Language.

[13]  K. Rayner,et al.  Psychology of Reading: 2nd Edition , 2012 .

[14]  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.

[15]  Albrecht W Inhoff,et al.  Visual word recognition during reading is followed by subvocal articulation. , 2010, Journal of experimental psychology. Learning, memory, and cognition.

[16]  Aaron J. Newman,et al.  Prosodic and narrative processing in American Sign Language: An fMRI study , 2010, NeuroImage.

[17]  Stephen M. Smith,et al.  General multilevel linear modeling for group analysis in FMRI , 2003, NeuroImage.

[18]  Yul-Wan Sung,et al.  Functional magnetic resonance imaging , 2004, Scholarpedia.

[19]  Karl J. Friston Models of brain function in neuroimaging. , 2005, Annual review of psychology.

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

[21]  D. Corcoran,et al.  An Acoustic Factor in Letter Cancellation , 1966, Nature.

[22]  R. Turner,et al.  Sentence Reading: A Functional MRI Study at 4 Tesla , 1997, Journal of Cognitive Neuroscience.

[23]  Trade-offs in detecting letters and comprehending text. , 2005, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[24]  Christine Chiarello,et al.  Right hemisphere language comprehension : perspectives from cognitive neuroscience , 1998 .

[25]  R. Klein,et al.  Influence of parafoveal processing on the missing-letter effect. , 2001, Journal of experimental psychology. Human perception and performance.

[26]  Paul Muter,et al.  Designing an Interface to Optimize Reading with Small Display Windows , 1999, Hum. Factors.

[27]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.

[28]  W. Simpson,et al.  Identification of the eye-brain-hand system with point processes: a new approach to simple reaction time. , 2000, Journal of experimental psychology. Human perception and performance.

[29]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[30]  C. D. Frith,et al.  Brain Activations during Visual Search: Contributions of Search Efficiency versus Feature Binding , 2003, NeuroImage.

[31]  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.

[32]  Letter detection for homographs with different meanings in different language texts , 2004, Bilingualism: Language and Cognition.

[33]  Jean Saint-Aubin,et al.  Eye movements as direct tests of the GO model for the missing-letter effect , 2007, Perception & psychophysics.

[34]  M. Masson Using confidence intervals for graphically based data interpretation. , 2003, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[35]  V. Walsh,et al.  Dissociating the contributions of human frontal eye fields and posterior parietal cortex to visual search. , 2011, Journal of neurophysiology.

[36]  C. A. Weaver,et al.  Psychology of Reading , 2012 .

[37]  R. C. Oldfield THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[38]  C. Price The anatomy of language: a review of 100 fMRI studies published in 2009 , 2010, Annals of the New York Academy of Sciences.

[39]  A. Healy,et al.  Detecting letters in continuous text: effects of display size. , 1987, Journal of experimental psychology. Human perception and performance.

[40]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[41]  Sharon M. Thomas,et al.  Assessing the importance of letter pairs in initial, exterior, and interior positions in reading. , 2003, Journal of experimental psychology. Learning, memory, and cognition.

[42]  R. Klein,et al.  One missing-letter effect: two methods of assessment. , 2004, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[43]  Jukka Hyönä,et al.  A morphological effect obtains for isolated words but not for words in sentence context , 2002 .

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

[45]  P. Indefrey A Meta‐analysis of Hemodynamic Studies on First and Second Language Processing: Which Suggested Differences Can We Trust and What Do They Mean? , 2006 .

[46]  Alexander Pollatsek,et al.  Psychology of reading, 2nd ed. , 2012 .

[47]  D. V. von Cramon,et al.  Syntactic comprehension in Parkinson's disease: investigating early automatic and late integrational processes using event-related brain potentials. , 2003, Neuropsychology.

[48]  C. F. Beckmann,et al.  Tensorial extensions of independent component analysis for multisubject FMRI analysis , 2005, NeuroImage.

[49]  Jean Saint-Aubin,et al.  Age changes in the missing-letter effect revisited. , 2005, Journal of experimental child psychology.

[50]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[51]  J. Saint-Aubin,et al.  The role of eye movements in the missing-letter effect revisited with the rapid serial visual presentation procedure. , 2010, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[52]  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.

[53]  Jean Saint-Aubin,et al.  Is Familiarity the All-Purpose Reading Tool? The Case of the Missing-Letter Effect for Self-Generated Texts , 2012 .

[54]  J. Cohen,et al.  Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. , 2000, Science.

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

[56]  Colin Humphries,et al.  Syntactic and Semantic Modulation of Neural Activity during Auditory Sentence Comprehension , 2006, Journal of Cognitive Neuroscience.

[57]  Michelle Hampson,et al.  Connectivity–behavior analysis reveals that functional connectivity between left BA39 and Broca's area varies with reading ability , 2006, NeuroImage.

[58]  Short Article: The Impact of Letter Detection on Eye Movement Patterns during Reading: Reconsidering Lexical Analysis in Connected Text as a Function of Task , 2006, Quarterly journal of experimental psychology.

[59]  S. Scott,et al.  Converging Language Streams in the Human Temporal Lobe , 2006, The Journal of Neuroscience.

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

[61]  Mark W. Woolrich,et al.  Fully Bayesian spatio-temporal modeling of FMRI data , 2004, IEEE Transactions on Medical Imaging.