Fixation-Related fMRI Analysis in the Domain of Reading Research: Using Self-Paced Eye Movements as Markers for Hemodynamic Brain Responses During Visual Letter String Processing

The present study investigated the feasibility of using self-paced eye movements during reading (measured by an eye tracker) as markers for calculating hemodynamic brain responses measured by functional magnetic resonance imaging (fMRI). Specifically, we were interested in whether the fixation-related fMRI analysis approach was sensitive enough to detect activation differences between reading material (words and pseudowords) and nonreading material (line and unfamiliar Hebrew strings). Reliable reading-related activation was identified in left hemisphere superior temporal, middle temporal, and occipito-temporal regions including the visual word form area (VWFA). The results of the present study are encouraging insofar as fixation-related analysis could be used in future fMRI studies to clarify some of the inconsistent findings in the literature regarding the VWFA. Our study is the first step in investigating specific visual word recognition processes during self-paced natural sentence reading via simultaneous eye tracking and fMRI, thus aiming at an ecologically valid measurement of reading processes. We provided the proof of concept and methodological framework for the analysis of fixation-related fMRI activation in the domain of reading research.

[1]  E. G. Jones Cerebral Cortex , 1987, Cerebral Cortex.

[2]  R. H. Baayen,et al.  The CELEX Lexical Database (CD-ROM) , 1996 .

[3]  Karl J. Friston,et al.  Human Brain Function , 1997 .

[4]  K. Rayner Eye movements in reading and information processing: 20 years of research. , 1998, Psychological bulletin.

[5]  S. Dehaene,et al.  Imaging unconscious semantic priming , 1998, Nature.

[6]  A M Dale,et al.  Optimal experimental design for event‐related fMRI , 1999, Human brain mapping.

[7]  S Lehéricy,et al.  The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. , 2000, Brain : a journal of neurology.

[8]  J B Poline,et al.  Cerebral mechanisms of word masking and unconscious repetition priming , 2001, Nature Neuroscience.

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

[10]  Karl J. Friston,et al.  Classical and Bayesian Inference in Neuroimaging: Applications , 2002, NeuroImage.

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

[12]  J. Fletcher,et al.  Brain mechanisms for reading words and pseudowords: an integrated approach. , 2002, Cerebral cortex.

[13]  Rna Henson,et al.  Analysis of fMRI time series: Linear Time-Invariant models, event-related fMRI and optimal experimental design , 2003 .

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

[15]  Karl J. Friston,et al.  A Dynamic Causal Modeling Study on Category Effects: BottomUp or TopDown Mediation? , 2003, Journal of Cognitive Neuroscience.

[16]  R. Goebel,et al.  Integration of Letters and Speech Sounds in the Human Brain , 2004, Neuron.

[17]  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.

[18]  M. Sigman,et al.  The neural code for written words: a proposal , 2005, Trends in Cognitive Sciences.

[19]  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.

[20]  Michael S. Beauchamp,et al.  Automatic Priming of Semantically Related Words Reduces Activity in the Fusiform Gyrus , 2005, Journal of Cognitive Neuroscience.

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

[22]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

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

[24]  Angela D. Friederici,et al.  Inhibition and facilitation in visual word recognition: Prefrontal contribution to the orthographic neighborhood size effect , 2007, NeuroImage.

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

[26]  Mario Braun,et al.  Welcome to the real world: Validating fixation-related brain potentials for ecologically valid settings , 2007, Brain Research.

[27]  Stanislas Dehaene,et al.  Task-specific change of unconscious neural priming in the cerebral language network , 2007, Proceedings of the National Academy of Sciences.

[28]  Mariano Sigman,et al.  Hierarchical Coding of Letter Strings in the Ventral Stream: Dissecting the Inner Organization of the Visual Word-Form System , 2007, Neuron.

[29]  Michele T. Diaz,et al.  Unconscious Word Processing Engages a Distributed Network of Brain Regions , 2007, Journal of Cognitive Neuroscience.

[30]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[31]  Bernard Mazoyer,et al.  Impact of modality and linguistic complexity during reading and listening tasks , 2007, NeuroImage.

[32]  Manuel Carreiras,et al.  Brain Activation for Lexical Decision and Reading Aloud: Two Sides of the Same Coin? , 2007, Journal of Cognitive Neuroscience.

[33]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

[34]  Jeffrey M. Zacks,et al.  Pictures of a thousand words: Investigating the neural mechanisms of reading with extremely rapid event-related fMRI , 2008, NeuroImage.

[35]  Stanislas Dehaene,et al.  Reading normal and degraded words: Contribution of the dorsal and ventral visual pathways , 2008, NeuroImage.

[36]  Ellen F. Lau,et al.  A cortical network for semantics: (de)constructing the N400 , 2008, Nature Reviews Neuroscience.

[37]  B. Shaywitz,et al.  Paying attention to reading: The neurobiology of reading and dyslexia , 2008, Development and Psychopathology.

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

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

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

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

[42]  Martin Kronbichler,et al.  A dual-route perspective on brain activation in response to visual words: Evidence for a length by lexicality interaction in the visual word form area (VWFA) , 2010, NeuroImage.

[43]  N. Kanwisher Functional specificity in the human brain: A window into the functional architecture of the mind , 2010, Proceedings of the National Academy of Sciences.

[44]  H. Wimmer,et al.  A Common Left Occipito-Temporal Dysfunction in Developmental Dyslexia and Acquired Letter-By-Letter Reading? , 2010, PloS one.

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

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

[47]  Silvia Brem,et al.  The left occipitotemporal system in reading: Disruption of focal fMRI connectivity to left inferior frontal and inferior parietal language areas in children with dyslexia , 2011, NeuroImage.

[48]  Jessica A. Turner,et al.  Behavioral Interpretations of Intrinsic Connectivity Networks , 2011, Journal of Cognitive Neuroscience.

[49]  Andreas Kleinschmidt,et al.  Specialization for written words over objects in the visual cortex , 2011, NeuroImage.

[50]  Timothy O. Laumann,et al.  Functional Network Organization of the Human Brain , 2011, Neuron.

[51]  A. Jacobs,et al.  Coregistration of eye movements and EEG in natural reading: analyses and review. , 2011, Journal of experimental psychology. General.

[52]  Cathy J. Price,et al.  Top-down modulation of ventral occipito-temporal responses during visual word recognition , 2011, NeuroImage.

[53]  H. Renvall,et al.  Functional Magnetic Resonance Imaging Blood Oxygenation Level-Dependent Signal and Magnetoencephalography Evoked Responses Yield Different Neural Functionality in Reading , 2011, The Journal of Neuroscience.

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

[55]  Erik D. Reichle,et al.  Direct lexical control of eye movements in reading: Evidence from a survival analysis of fixation durations , 2012, Cognitive Psychology.

[56]  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.

[57]  Frans W Cornelissen,et al.  Fixation based event‐related fmri analysis: Using eye fixations as events in functional magnetic resonance imaging to reveal cortical processing during the free exploration of visual images , 2012, Human Brain Mapping.

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

[59]  A. Jacobs,et al.  Stimulus onset asynchrony and the timeline of word recognition: Event-related potentials during sentence reading , 2012, Neuropsychologia.

[60]  K. Amunts,et al.  Effects of lexicality and word frequency on brain activation in dyslexic readers , 2013, Brain and Language.