Context-dependent lexical ambiguity resolution: MEG evidence for the time-course of activity in left inferior frontal gyrus and posterior middle temporal gyrus

&NA; An MEG study investigated the role of context in semantic interpretation by examining the comprehension of ambiguous words in contexts leading to different interpretations. We compared high‐ambiguity words in minimally different contexts (to bowl, the bowl) to low‐ambiguity counterparts (the tray, to flog). Whole brain beamforming revealed the engagement of left inferior frontal gyrus (LIFG) and posterior middle temporal gyrus (LPMTG). Points of interest analyses showed that both these sites showed a stronger response to verb‐contexts by 200 ms post‐stimulus and displayed overlapping ambiguity effects that were sustained from 300 ms onwards. The effect of context was stronger for high‐ambiguity words than for low‐ambiguity words at several different time points, including within the first 100 ms post‐stimulus. Unlike LIFG, LPMTG also showed stronger responses to verb than noun contexts in low‐ambiguity trials. We argue that different functional roles previously attributed to LIFG and LPMTG are in fact played out at different periods during processing.

[1]  P. Hagoort Impairments of Lexical-Semantic Processing in Aphasia: Evidence from the Processing of Lexical Ambiguities , 1993, Brain and Language.

[2]  F. Carducci,et al.  Automatic alignment of EEG/MEG and MRI data sets , 2001, Clinical Neurophysiology.

[3]  John Sinclair,et al.  Collins COBUILD English Language Dictionary , 1987 .

[4]  P. Fletcher,et al.  Neural processing of nouns and verbs: the role of inflectional morphology , 2004, Neuropsychologia.

[5]  Adrian L. Williams,et al.  Task-Related Changes in Cortical Synchronization Are Spatially Coincident with the Hemodynamic Response , 2002, NeuroImage.

[6]  W. John Boscardin,et al.  SAS® for mixed models (2nd edn). Ramon C. Littell, George A. Milliken, Walter W. Stroup, Russell D. Wolfinger and Oliver Schabenberger, SAS Institute, Cary, NC, 2006. No. of pages: xii + 814. Price: $89.95. ISBN 10: 1-59047-500-3; ISBN 13: 978-1-59047-500-3 , 2007 .

[7]  P. Nunez,et al.  Spatial‐temporal structures of human alpha rhythms: Theory, microcurrent sources, multiscale measurements, and global binding of local networks , 2001, Human brain mapping.

[8]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

[9]  W. Marslen-Wilson,et al.  Making Sense of Semantic Ambiguity: Semantic Competition in Lexical Access , 2002 .

[10]  R M Leahy,et al.  A sensor-weighted overlapping-sphere head model and exhaustive head model comparison for MEG. , 1999, Physics in medicine and biology.

[11]  Elizabeth Jefferies,et al.  Shared neural processes support semantic control and action understanding , 2015, Brain and Language.

[12]  M. L. Lambon Ralph,et al.  The Neural Organization of Semantic Control: TMS Evidence for a Distributed Network in Left Inferior Frontal and Posterior Middle Temporal Gyrus , 2010, Cerebral cortex.

[13]  Jonathan Grainger,et al.  Early Activity in Broca's Area During Reading Reflects Fast Access to Articulatory Codes From Print. , 2015, Cerebral cortex.

[14]  P. Hagoort On Broca, brain, and binding: a new framework , 2005, Trends in Cognitive Sciences.

[15]  Tianzi Jiang,et al.  Tractography-based Parcellation of the Human Middle Temporal Gyrus , 2015, Scientific Reports.

[16]  Qiang Wei,et al.  Lexical access and selection of contextually appropriate meaning for ambiguous words , 2007, NeuroImage.

[17]  Katsuyuki Sakai,et al.  Prefrontal Set Activity Predicts Rule-Specific Neural Processing during Subsequent Cognitive Performance , 2006, The Journal of Neuroscience.

[18]  Sharon L. Thompson-Schill,et al.  Conceptual Representations of Action in the Lateral Temporal Cortex , 2005, Journal of Cognitive Neuroscience.

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

[20]  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.

[21]  L. Pylkkänen,et al.  Basic linguistic composition recruits the left anterior temporal lobe and left angular gyrus during both listening and reading. , 2013, Cerebral cortex.

[22]  Kara D. Federmeier,et al.  To mind the mind: An event-related potential study of word class and semantic ambiguity , 2006, Brain Research.

[23]  W. Drongelen,et al.  Localization of brain electrical activity via linearly constrained minimum variance spatial filtering , 1997, IEEE Transactions on Biomedical Engineering.

[24]  R. Wolfinger,et al.  SAS for Mixed Models , 2018 .

[25]  Elizabeth Jefferies,et al.  Going beyond Inferior Prefrontal Involvement in Semantic Control: Evidence for the Additional Contribution of Dorsal Angular Gyrus and Posterior Middle Temporal Cortex , 2013, Journal of Cognitive Neuroscience.

[26]  Alex Martin,et al.  Semantic memory and the brain: structure and processes , 2001, Current Opinion in Neurobiology.

[27]  Marie Bienkowski,et al.  Automatic access of the meanings of ambiguous words in context: Some limitations of knowledge-based processing , 1982, Cognitive Psychology.

[28]  Piers L. Cornelissen,et al.  Interactions between visual and semantic processing during object recognition revealed by modulatory effects of age of acquisition , 2014, NeuroImage.

[29]  D. Perani,et al.  The neural correlates of verb and noun processing. A PET study. , 1999, Brain : a journal of neurology.

[30]  M. Bastiaansen,et al.  Fast oscillatory dynamics during language comprehension: Unification versus maintenance and prediction? , 2015, Brain and Language.

[31]  Matthew F Glasser,et al.  DTI tractography of the human brain's language pathways. , 2008, Cerebral cortex.

[32]  S. Hanslmayr,et al.  Oscillatory power decreases and long-term memory: the information via desynchronization hypothesis , 2012, Front. Hum. Neurosci..

[33]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[34]  E. Jefferies The neural basis of semantic cognition: Converging evidence from neuropsychology, neuroimaging and TMS , 2013, Cortex.

[35]  W. Sommer,et al.  Partial advance information and response preparation: inferences from the lateralized readiness potential. , 1996, Journal of experimental psychology. General.

[36]  A. Ellis,et al.  Oscillatory Dynamics Supporting Semantic Cognition: MEG Evidence for the Contribution of the Anterior Temporal Lobe Hub and Modality-Specific Spokes , 2017, PloS one.

[37]  Dirk P. Janssen,et al.  Twice random, once mixed: Applying mixed models to simultaneously analyze random effects of language and participants , 2011, Behavior Research Methods.

[38]  B. Staresina,et al.  Oscillations and Episodic Memory: Addressing the Synchronization/Desynchronization Conundrum , 2016, Trends in Neurosciences.

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

[40]  Justin C. Hulbert,et al.  Understanding words in context: The role of Broca's area in word comprehension , 2007, Brain Research.

[41]  K. Bäuml,et al.  The Relationship between Brain Oscillations and BOLD Signal during Memory Formation: A Combined EEG–fMRI Study , 2011, The Journal of Neuroscience.

[42]  Elizabeth Jefferies,et al.  Fractionating the anterior temporal lobe: MVPA reveals differential responses to input and conceptual modality , 2017, NeuroImage.

[43]  Volkmar Glauche,et al.  Ventral and dorsal pathways for language , 2008, Proceedings of the National Academy of Sciences.

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

[45]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

[46]  Peter F. Liddle,et al.  Changes in brain network activity during working memory tasks: A magnetoencephalography study , 2011, NeuroImage.

[47]  Silvia P. Gennari,et al.  Motion and actions in language: Semantic representations in occipito-temporal cortex , 2013, Brain and Language.

[48]  Friedemann Pulvermüller,et al.  Understanding in an instant: Neurophysiological evidence for mechanistic language circuits in the brain , 2009, Brain and Language.

[49]  J. Schoffelen,et al.  Beta oscillations relate to the N400m during language comprehension , 2012, Human brain mapping.

[50]  R. Adolphs,et al.  NEURAL CORRELATES OF CONCEPTUAL KNOWLEDGE FOR ACTIONS , 2003, Cognitive neuropsychology.

[51]  Lalu Mansinha,et al.  Localization of the complex spectrum: the S transform , 1996, IEEE Trans. Signal Process..

[52]  Arjan Hillebrand,et al.  Beamformer analysis of MEG data. , 2005, International review of neurobiology.

[53]  Liina Pylkkänen,et al.  The role of the left anterior temporal lobe in semantic composition vs. semantic memory , 2014, Neuropsychologia.

[54]  P. Tabossi Effects of context on the immediate interpretation of unambiguous nouns. , 1988 .

[55]  T. Rogers,et al.  The neural and computational bases of semantic cognition , 2016, Nature Reviews Neuroscience.

[56]  Robin K. Morris,et al.  Lexical ambiguity and fixation times in reading , 1988 .

[57]  Kara D. Federmeier,et al.  Brain responses to nouns, verbs and class-ambiguous words in context. , 2000, Brain : a journal of neurology.

[58]  Billi Randall,et al.  Cortical Differentiation for Nouns and Verbs Depends on Grammatical Markers , 2008, Journal of Cognitive Neuroscience.

[59]  Jia-Hong Gao,et al.  Neural systems for word meaning modulated by semantic ambiguity , 2004, NeuroImage.

[60]  J. Smallwood,et al.  Automatic and Controlled Semantic Retrieval: TMS Reveals Distinct Contributions of Posterior Middle Temporal Gyrus and Angular Gyrus , 2015, The Journal of Neuroscience.

[61]  S. Cappa,et al.  Nouns and verbs in the brain: A review of behavioural, electrophysiological, neuropsychological and imaging studies , 2011, Neuroscience & Biobehavioral Reviews.

[62]  Gary G. R. Green,et al.  Source stability index: A novel beamforming based localisation metric , 2010, NeuroImage.

[63]  W. Klimesch EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[64]  L. M. Ward,et al.  Synchronous neural oscillations and cognitive processes , 2003, Trends in Cognitive Sciences.

[65]  Matthew H. Davis,et al.  Dissociating frontotemporal contributions to semantic ambiguity resolution in spoken sentences. , 2012, Cerebral cortex.

[66]  Maryellen C. MacDonald,et al.  The lexical nature of syntactic ambiguity resolution , 1994 .

[67]  Jennifer M. Rodd,et al.  The functional organisation of the fronto-temporal language system: Evidence from syntactic and semantic ambiguity , 2010, Neuropsychologia.

[68]  Derek K. Jones,et al.  Virtual in Vivo Interactive Dissection of White Matter Fasciculi in the Human Brain , 2002, NeuroImage.

[69]  Thomas E. Nichols,et al.  Nonparametric Permutation Tests for Functional Neuroimaging , 2003 .

[70]  Alfonso Caramazza,et al.  Dissociating neural correlates for nouns and verbs , 2005, NeuroImage.

[71]  David Badre,et al.  Semantic retrieval, mnemonic control, and prefrontal cortex. , 2002, Behavioral and cognitive neuroscience reviews.

[72]  Marcel Adam Just,et al.  From the SelectedWorks of Marcel Adam Just 2007 Lexical ambiguity in sentence comprehension , 2016 .

[73]  Gary G. R. Green,et al.  Non-parametric statistical thresholding of baseline free MEG beamformer images , 2011, NeuroImage.

[74]  A. Caramazza,et al.  Concepts Are More than Percepts: The Case of Action Verbs , 2008, The Journal of Neuroscience.

[75]  Elizabeth Jefferies,et al.  Charting the effects of TMS with fMRI: Modulation of cortical recruitment within the distributed network supporting semantic control , 2016, Neuropsychologia.

[76]  Alfonso Caramazza,et al.  Grammatical processing of nouns and verbs in left frontal cortex? , 2003, Neuropsychologia.

[77]  Matthew J. Brookes,et al.  Optimising experimental design for MEG beamformer imaging , 2008, NeuroImage.

[78]  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.

[79]  Maryellen C. MacDonald,et al.  Context-dependent interpretation of words: Evidence for interactive neural processes , 2007, NeuroImage.

[80]  Alfonso Caramazza,et al.  Grammatical Distinctions in the Left Frontal Cortex , 2001, Journal of Cognitive Neuroscience.

[81]  Timothy E. J. Behrens,et al.  The evolution of the arcuate fasciculus revealed with comparative DTI , 2008, Nature Neuroscience.

[82]  M-X Huang,et al.  Commonalities and Differences Among Vectorized Beamformers in Electromagnetic Source Imaging , 2003, Brain Topography.

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

[84]  M. Bastiaansen,et al.  A predictive coding framework for rapid neural dynamics during sentence-level language comprehension , 2015, Cortex.

[85]  J. Kable,et al.  Neural Substrates of Action Event Knowledge , 2002, Journal of Cognitive Neuroscience.

[86]  E. Halgren,et al.  Dynamic Statistical Parametric Mapping Combining fMRI and MEG for High-Resolution Imaging of Cortical Activity , 2000, Neuron.

[87]  Elizabeth Jefferies,et al.  Exploring the role of the posterior middle temporal gyrus in semantic cognition: Integration of anterior temporal lobe with executive processes , 2016, NeuroImage.

[88]  Elizabeth Jefferies,et al.  Both the Middle Temporal Gyrus and the Ventral Anterior Temporal Area Are Crucial for Multimodal Semantic Processing: Distortion-corrected fMRI Evidence for a Double Gradient of Information Convergence in the Temporal Lobes , 2012, Journal of Cognitive Neuroscience.

[89]  J D Watson,et al.  Nonparametric Analysis of Statistic Images from Functional Mapping Experiments , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[90]  F. Pulvermüller,et al.  Spatiotemporal Signatures of Large-Scale Synfire Chains for Speech Processing as Revealed by MEG , 2008, Cerebral cortex.

[91]  G. Simpson Lexical ambiguity and its role in models of word recognition. , 1984, Psychological bulletin.

[92]  James Davey Exploring the role of the posterior middle temporal gyrus in semantic cognition: Integration of anterior temporal lobe with goal-oriented cognition , 2016 .

[93]  Morten L. Kringelbach,et al.  Visual word recognition: the first half second , 2004, NeuroImage.

[94]  Peter Hagoort,et al.  Neural activity during sentence processing as reflected in theta, alpha, beta, and gamma oscillations , 2016, NeuroImage.

[95]  P. Hagoort Nodes and networks in the neural architecture for language: Broca's region and beyond , 2014, Current Opinion in Neurobiology.