Dynamic Causal Modeling of Spatiotemporal Integration of Phonological and Semantic Processes: An Electroencephalographic Study

Integration of phonological and lexicosemantic processes is essential for visual word recognition. Here we used dynamic causal modeling of event-related potentials, combined with group source reconstruction, to estimate how those processes translate into context-dependent modulation of effective connectivity within the temporal-frontal language network. Fifteen healthy human subjects performed a phoneme detection task in pseudo-words and a semantic categorization task in words. Cortical current densities revealed the sequential activation of temporal regions, from the occipital–temporal junction toward the anterior temporal lobe, before reaching the inferior frontal gyrus. A difference of activation between phonology and semantics was identified in the anterior temporal lobe within the 240–300 ms peristimulus time window. Dynamic causal modeling indicated this increase of activation of the anterior temporal lobe in the semantic condition as a consequence of an increase of forward connectivity from the posterior inferior temporal lobe to the anterior temporal lobe. In addition, fast activation of the inferior frontal region, which allowed a feedback control of frontal regions on the superior temporal and posterior inferior temporal cortices, was found to be likely. Our results precisely describe spatiotemporal network mechanisms occurring during integration of phonological and semantic processes. In particular, they support the hypothesis of multiple pathways within the temporal lobe for language processing, where frontal regions would exert a top-down control on temporal regions in the recruitment of the anterior temporal lobe for semantic processing.

[1]  P Celsis,et al.  Automatic grapheme processing in the left occipitotemporal cortex , 2002, Neuroreport.

[2]  Marc Brysbaert,et al.  Lexique 2 : A new French lexical database , 2004, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

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

[4]  R. Salmelin,et al.  Dynamics of visual feature analysis and object-level processing in face versus letter-string perception. , 2002, Brain : a journal of neurology.

[5]  J. Fletcher,et al.  Brain mechanisms for reading: the role of the superior temporal gyrus in word and pseudoword naming , 2000, Neuroreport.

[6]  B. Argall,et al.  Integration of Auditory and Visual Information about Objects in Superior Temporal Sulcus , 2004, Neuron.

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

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

[9]  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.

[10]  M. Mintun,et al.  Regional cerebral blood flow during word and nonword reading , 1997, Human brain mapping.

[11]  R J Wise,et al.  Separate neural subsystems within 'Wernicke's area'. , 2001, Brain : a journal of neurology.

[12]  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.

[13]  Joseph Dien,et al.  The neurocognitive basis of reading single words as seen through early latency ERPs: A model of converging pathways , 2009, Biological Psychology.

[14]  Richard S. J. Frackowiak,et al.  A voxel‐based morphometry study of semantic dementia: Relationship between temporal lobe atrophy and semantic memory , 2000, Annals of neurology.

[15]  B. Mesquita,et al.  Adjustment to Chronic Diseases and Terminal Illness Health Psychology : Psychological Adjustment to Chronic Disease , 2006 .

[16]  Karl J. Friston,et al.  Multiple sparse priors for the M/EEG inverse problem , 2008, NeuroImage.

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

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

[19]  D. Pandya,et al.  Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. , 2005, Cerebral cortex.

[20]  T. Rogers,et al.  Where do you know what you know? The representation of semantic knowledge in the human brain , 2007, Nature Reviews Neuroscience.

[21]  Karl J. Friston,et al.  Statistical parametric mapping , 2013 .

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

[23]  Elizabeth Jefferies,et al.  Semantic Processing in the Anterior Temporal Lobes: A Meta-analysis of the Functional Neuroimaging Literature , 2010, Journal of Cognitive Neuroscience.

[24]  Friedemann Pulvermüller,et al.  The Word Processing Deficit in Semantic Dementia: All Categories Are Equal, but Some Categories Are More Equal than Others , 2010, Journal of Cognitive Neuroscience.

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

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

[27]  E. Crosby,et al.  Correlative Anatomy of the Nervous System , 1962 .

[28]  R. Poldrack,et al.  Dissociable Controlled Retrieval and Generalized Selection Mechanisms in Ventrolateral Prefrontal Cortex , 2005, Neuron.

[29]  Alfonso Caramazza,et al.  The role of phonological and orthographic information in lexical selection , 2003, Brain and Language.

[30]  D J Mikulis,et al.  Functional MRI of phonological and semantic processing in temporal lobe epilepsy. , 2001, Brain : a journal of neurology.

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

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

[33]  S. Petersen,et al.  Effects of Lexicality, Frequency, and Spelling-to-Sound Consistency on the Functional Anatomy of Reading , 1999, Neuron.

[34]  E. Halgren,et al.  Top-down facilitation of visual recognition. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[35]  M. Bar.  A Cortical Mechanism for Triggering Top-Down Facilitation in Visual Object Recognition , 2003, Journal of Cognitive Neuroscience.

[36]  L. Tyler,et al.  Unitary vs multiple semantics: PET studies of word and picture processing , 2004, Brain and Language.

[37]  Karl J. Friston,et al.  Topological inference for EEG and MEG , 2010, 1011.2901.

[38]  Irene P. Kan,et al.  Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[40]  Karl J. Friston,et al.  Electromagnetic source reconstruction for group studies , 2008, NeuroImage.

[41]  J. T. Lurito,et al.  Comparison of Rhyming and Word Generation with FMRI , 1998, NeuroImage.

[42]  S. Petersen,et al.  A procedure for identifying regions preferentially activated by attention to semantic and phonological relations using functional magnetic resonance imaging , 2003, Neuropsychologia.

[43]  Karl J. Friston,et al.  Bayesian model selection for group studies , 2009, NeuroImage.

[44]  Charles D. Smith,et al.  Dissociation of Automatic and Strategic Lexical-Semantics: Functional Magnetic Resonance Imaging Evidence for Differing Roles of Multiple Frontotemporal Regions , 2006, The Journal of Neuroscience.

[45]  Richard S. J. Frackowiak,et al.  Functional anatomy of a common semantic system for words and pictures , 1996, Nature.

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

[47]  James L. McClelland,et al.  A distributed, developmental model of word recognition and naming. , 1989, Psychological review.

[48]  S. Dehaene,et al.  Direct Intracranial, fMRI, and Lesion Evidence for the Causal Role of Left Inferotemporal Cortex in Reading , 2006, Neuron.

[49]  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.

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

[51]  Karl J. Friston,et al.  Canonical Source Reconstruction for MEG , 2007, Comput. Intell. Neurosci..

[52]  Asaid Khateb,et al.  Variability of fMRI activation during a phonological and semantic language task in healthy subjects , 2004, Human brain mapping.

[53]  Mark S. Seidenberg,et al.  Computing the meanings of words in reading: cooperative division of labor between visual and phonological processes. , 2004, Psychological review.

[54]  G. A. Calvert,et al.  Auditory-visual processing represented in the human superior temporal gyrus , 2007, Neuroscience.

[55]  Richard J. Binney,et al.  The ventral and inferolateral aspects of the anterior temporal lobe are crucial in semantic memory: evidence from a novel direct comparison of distortion-corrected fMRI, rTMS, and semantic dementia. , 2010, Cerebral cortex.

[56]  L. Koessler,et al.  Spatial localization of EEG electrodes , 2007, Neurophysiologie Clinique/Clinical Neurophysiology.

[57]  M. L. Lambon Ralph,et al.  Conceptual knowledge is underpinned by the temporal pole bilaterally: convergent evidence from rTMS. , 2009, Cerebral cortex.

[58]  Stanislas Dehaene,et al.  Specialization within the ventral stream: the case for the visual word form area , 2004, NeuroImage.

[59]  Derek K. Jones,et al.  Occipito-temporal connections in the human brain. , 2003, Brain : a journal of neurology.

[60]  M. Baciu,et al.  Functional MRI evidence for modulation of cerebral activity by grapheme-to-phoneme conversion in French, and by the variable of gender , 2011, Journal of Neurolinguistics.

[61]  Victor W. Henderson,et al.  Anatomy of posterior pathways in reading: A reassessment , 1986, Brain and Language.

[62]  S. Greenblatt,et al.  Subangular alexia without agraphia or hemianopsia , 1976, Brain and Language.

[63]  Nelson J. Trujillo-Barreto,et al.  Bayesian model averaging in EEG/MEG imaging , 2004, NeuroImage.

[64]  Karl J. Friston,et al.  A multimodal language region in the ventral visual pathway , 1998, Nature.

[65]  T. Allison,et al.  Word recognition in the human inferior temporal lobe , 1994, Nature.

[66]  S. Thompson-Schill,et al.  The frontal lobes and the regulation of mental activity , 2005, Current Opinion in Neurobiology.

[67]  Alan C. Evans,et al.  Lateralization of phonetic and pitch discrimination in speech processing. , 1992, Science.

[68]  S. Bookheimer,et al.  Form and Content Dissociating Syntax and Semantics in Sentence Comprehension , 1999, Neuron.

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

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

[71]  G. Chételat,et al.  Spoken Word Memory Traces within the Human Auditory Cortex Revealed by Repetition Priming and Functional Magnetic Resonance Imaging , 2008, The Journal of Neuroscience.

[72]  Uta Noppeney,et al.  Temporal lobe lesions and semantic impairment: a comparison of herpes simplex virus encephalitis and semantic dementia. , 2006, Brain : a journal of neurology.

[73]  Ayumu Matani,et al.  Early neural activation for lexico-semantic access in the left anterior temporal area analyzed by an fMRI-assisted MEG multidipole method , 2009, NeuroImage.

[74]  S. Wakana,et al.  Fiber tract-based atlas of human white matter anatomy. , 2004, Radiology.

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

[76]  M. Weiner,et al.  Cognition and anatomy in three variants of primary progressive aphasia , 2004, Annals of neurology.

[77]  Todd B. Parrish,et al.  Language network specializations: An analysis with parallel task designs and functional magnetic resonance imaging , 2005, NeuroImage.

[78]  E. Rolls,et al.  The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology , 2004, Progress in Neurobiology.

[79]  H. Barbas.  Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices , 2000, Brain Research Bulletin.

[80]  Katrin Amunts,et al.  White matter fiber tracts of the human brain: Three-dimensional mapping at microscopic resolution, topography and intersubject variability , 2006, NeuroImage.

[81]  R. Berndt,et al.  Functional pronunciation units in English words. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

[82]  Sven Joubert,et al.  Grapheme-phoneme processing of single words , 2001, Brain and Cognition.

[83]  Daniel Brandeis,et al.  Neurophysiological signs of rapidly emerging visual expertise for symbol strings , 2005, Neuroreport.

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

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

[86]  Grégory Simon,et al.  Orthographic transparency and grapheme–phoneme conversion: An ERP study in Arabic and French readers , 2006, Brain Research.

[87]  Valerie A. Carr,et al.  Spatiotemporal Dynamics of Modality-Specific and Supramodal Word Processing , 2003, Neuron.

[88]  Ferath Kherif,et al.  Automatic Top-Down Processing Explains Common Left Occipito-Temporal Responses to Visual Words and Objects , 2010, Cerebral cortex.

[89]  Laurent Lamalle,et al.  Functional MRI approach for assessing hemispheric predominance of regions activated by a phonological and a semantic task. , 2007, European journal of radiology.

[90]  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.