Building phrases in language production: An MEG study of simple composition

Although research on language production has developed detailed maps of the brain basis of single word production in both time and space, little is known about the spatiotemporal dynamics of the processes that combine individual words into larger representations during production. Studying composition in production is challenging due to difficulties both in controlling produced utterances and in measuring the associated brain responses. Here, we circumvent both problems using a minimal composition paradigm combined with the high temporal resolution of magnetoencephalography (MEG). With MEG, we measured the planning stages of simple adjective-noun phrases ('red tree'), matched list controls ('red, blue'), and individual nouns ('tree') and adjectives ('red'), with results indicating combinatorial processing in the ventro-medial prefrontal cortex (vmPFC) and left anterior temporal lobe (LATL), two regions previously implicated for the comprehension of similar phrases. These effects began relatively quickly (∼180 ms) after the presentation of a production prompt, suggesting that combination commences with initial lexical access. Further, while in comprehension, vmPFC effects have followed LATL effects, in this production paradigm vmPFC effects occurred mostly in parallel with LATL effects, suggesting that a late process in comprehension is an early process in production. Thus, our results provide a novel neural bridge between psycholinguistic models of comprehension and production that posit functionally similar combinatorial mechanisms operating in reversed order.

[1]  S. Zeki,et al.  Three cortical stages of colour processing in the human brain. , 1998, Brain : a journal of neurology.

[2]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[3]  W. Grodd,et al.  The speaking brain: a tutorial introduction to fMRI experiments in the production of speech, prosody and syntax , 2002, Journal of Neurolinguistics.

[4]  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.

[5]  Michael J Gardner,et al.  In Response. , 2015, Journal of orthopaedic trauma.

[6]  L. Pylkkänen,et al.  Processing psych verbs: Behavioural and MEG measures of two different types of semantic complexity , 2010 .

[7]  K. Amunts,et al.  Left cytoarchitectonic area 44 supports selection in the mental lexicon during language production , 2009, Brain Structure and Function.

[8]  W. Levelt,et al.  The spatial and temporal signatures of word production components , 2004, Cognition.

[9]  Mark C. W. van Rossum,et al.  Systematic biases in early ERP and ERF components as a result of high-pass filtering , 2012, Journal of Neuroscience Methods.

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

[11]  S. Dehaene,et al.  Cortical representation of the constituent structure of sentences , 2011, Proceedings of the National Academy of Sciences.

[12]  Sarah M. E. Gierhan,et al.  Shared Language , 2011, Psychological science.

[13]  A. Nobre,et al.  The Response of Left Temporal Cortex to Sentences , 2002, Journal of Cognitive Neuroscience.

[14]  Peter Hagoort,et al.  Neural responses to the production and comprehension of syntax in identical utterances , 2004, Brain and Language.

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

[16]  A. A. Wijers,et al.  Localizing components of a complex task: sentence processing and working memory , 1998, Neuroreport.

[17]  R. Salmelin Clinical neurophysiology of language: The MEG approach , 2007, Clinical Neurophysiology.

[18]  U. Hasson,et al.  Speaker–listener neural coupling underlies successful communication , 2010, Proceedings of the National Academy of Sciences.

[19]  Antje S. Meyer,et al.  An MEG Study of Picture Naming , 1998, Journal of Cognitive Neuroscience.

[20]  T. Zimmermann Free Choice Disjunction and Epistemic Possibility , 2000 .

[21]  A. Syrota,et al.  The Cortical Representation of Speech , 1993, Journal of Cognitive Neuroscience.

[22]  Lyn Frazier,et al.  Theories of sentence processing , 1987 .

[23]  D. Swinney,et al.  Response of anterior temporal cortex to syntactic and prosodic manipulations during sentence processing , 2005, Human brain mapping.

[24]  D. Shohamy,et al.  Ventromedial prefrontal-subcortical systems and the generation of affective meaning , 2012, Trends in Cognitive Sciences.

[25]  Emily B. Myers,et al.  The role of the left inferior frontal gyrus in implicit semantic competition and selection: An event-related fMRI study , 2008, Brain Research.

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

[27]  Randy L. Buckner,et al.  An Event-Related fMRI Study of Overt and Covert Word Stem Completion , 2001, NeuroImage.

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

[29]  Liina Pylkkänen,et al.  An MEG Study of Silent Meaning , 2007, Journal of Cognitive Neuroscience.

[30]  Liina Pylkkänen,et al.  The time-course and spatial distribution of brain activity associated with sentence processing , 2012, NeuroImage.

[31]  Marc Ouellet,et al.  Parallel processing of objects in a naming task. , 2008, Journal of experimental psychology. Learning, memory, and cognition.

[32]  Antje S Meyer,et al.  The time course of name retrieval during multiple-object naming: evidence from extrafoveal-on-foveal effects. , 2010, Journal of experimental psychology. Learning, memory, and cognition.

[33]  Mary C. Potter,et al.  Understanding noun phrases , 1979 .

[34]  W. Levelt,et al.  Speaking: From Intention to Articulation , 1990 .

[35]  F.-Xavier Alario,et al.  Frequency effects in noun phrase production: Implications for models of lexical access , 2002 .

[36]  S. Scott,et al.  A Common System for the Comprehension and Production of Narrative Speech , 2007, The Journal of Neuroscience.

[37]  M. Pickering,et al.  An integrated theory of language production and comprehension. , 2013, The Behavioral and brain sciences.

[38]  J. Fiez,et al.  Functional heterogeneity within Broca's area during verbal working memory , 2002, Physiology & Behavior.

[39]  Andrea E. Martin,et al.  The Anterior Midline Field: coercion or decision making? , 2009 .

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

[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]  A. Friederici,et al.  Broca's area in the human brain is involved in the selection of grammatical gender for language production: evidence from event-related functional magnetic resonance imaging , 2002, Neuroscience Letters.

[43]  Gregory Hickok,et al.  Selective attention to semantic and syntactic features modulates sentence processing networks in anterior temporal cortex. , 2009, Cerebral cortex.

[44]  Albert Costa,et al.  Riding the Lexical Speedway: A Critical Review on the Time Course of Lexical Selection in Speech Production , 2011, Front. Psychology.

[45]  Liina Pylkkänen,et al.  Combination Across Domains: An MEG Investigation into the Relationship between Mathematical, Pictorial, and Linguistic Processing , 2013, Front. Psychology.

[46]  M. Erb,et al.  Overt sentence production in event-related fMRI , 2005, Neuropsychologia.

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

[48]  L. Pylkkänen,et al.  Semantics vs. world knowledge in prefrontal cortex , 2009 .

[49]  R. Mar The neuropsychology of narrative: story comprehension, story production and their interrelation , 2004, Neuropsychologia.

[50]  Liina Pylkkänen,et al.  Simple Composition: A Magnetoencephalography Investigation into the Comprehension of Minimal Linguistic Phrases , 2011, The Journal of Neuroscience.

[51]  Liina Pylkkänen,et al.  Grounding the cognitive neuroscience of semantics in linguistic theory , 2011 .

[52]  M. Pickering,et al.  Structural priming: a critical review. , 2008, Psychological bulletin.

[53]  S. Kitazawa,et al.  Neural correlates of tactile temporal-order judgment in humans: an fMRI study. , 2013, Cerebral cortex.

[54]  Willem J. M. Levelt,et al.  Effects of syllable frequency in speech production , 2006, Cognition.

[55]  E. Maguire,et al.  The functional neuroanatomy of comprehension and memory: the importance of prior knowledge. , 1999, Brain : a journal of neurology.

[56]  Iain D. Gilchrist,et al.  Testing a Simplified Method for Measuring Velocity Integration in Saccades Using a Manipulation of Target Contrast , 2011, Front. Psychology.

[57]  Peter Hagoort,et al.  Retrieval and unification of syntactic structure in sentence comprehension: an FMRI study using word-category ambiguity. , 2009, Cerebral cortex.

[58]  A Wingfield,et al.  Response Latencies in Naming Objects , 1965, The Quarterly journal of experimental psychology.

[59]  Olaf Hauk,et al.  Electroencephalographic activity over temporal brain areas during phonological encoding in picture naming , 2000, Clinical Neurophysiology.

[60]  H. Schriefers,et al.  Parallelism in the Production of Noun Phrases: Experiments and Reaction Time Models. , 1999 .

[61]  P Hagoort,et al.  A neural correlate of syntactic encoding during speech production , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Bernadette M. Jansma,et al.  Neural correlates of conceptualisation difficulty during the preparation of complex utterances , 2007 .

[63]  A. Braun,et al.  The neural organization of discourse: an H2 15O-PET study of narrative production in English and American sign language. , 2001, Brain : a journal of neurology.

[64]  A. Meyer Lexical Access in Phrase and Sentence Production: Results from Picture–Word Interference Experiments , 1996 .

[65]  W. Levelt,et al.  Semantic Category Interference in Overt Picture Naming: Sharpening Current Density Localization by PCA , 2002, Journal of Cognitive Neuroscience.

[66]  Liina Pylkkänen,et al.  journal homepage: www.elsevier.com/locate/b&l Processing events: Behavioral and neuromagnetic correlates of Aspectual Coercion , 2022 .

[67]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[68]  Fernanda Ferreira,et al.  Syntax in Language Production: An Approach Using Tree-Adjoining Grammars , 2011 .

[69]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[70]  Thomas F Münte,et al.  Neurophysiological correlates of linearization in language production , 2008, BMC Neuroscience.

[71]  Curt Burgess,et al.  Producing high-dimensional semantic spaces from lexical co-occurrence , 1996 .

[72]  Emily J. Mayberry,et al.  Coherent concepts are computed in the anterior temporal lobes , 2010, Proceedings of the National Academy of Sciences.

[73]  Mark C. Smith,et al.  Horizontal information flow in spoken sentence production. , 2004, Journal of experimental psychology. Learning, memory, and cognition.

[74]  M. Raichle,et al.  Anatomic Localization and Quantitative Analysis of Gradient Refocused Echo-Planar fMRI Susceptibility Artifacts , 1997, NeuroImage.

[75]  Rasha Abdel Rahman,et al.  Electrophysiological Chronometry of Semantic Context Effects in Language Production , 2011, Journal of Cognitive Neuroscience.

[76]  Laura Monetta,et al.  The role of the left anterior temporal lobe in the semantic processing of famous faces , 2010, NeuroImage.

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

[78]  C. D. Frith,et al.  The Role of the Dorsolateral Prefrontal Cortex: Evidence from the Effects of Contextual Constraint in a Sentence Completion Task , 2002, NeuroImage.

[79]  Liina Pylkkänen,et al.  Flexible Composition: Meg Evidence for the Deployment of Basic Combinatorial Linguistic Mechanisms in Response to Task Demands Flexible Composition (meg) , 2022 .

[80]  A. Friederici Towards a neural basis of auditory sentence processing , 2002, Trends in Cognitive Sciences.

[81]  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.

[82]  Jiang Xu,et al.  Language in context: emergent features of word, sentence, and narrative comprehension , 2005, NeuroImage.

[83]  Elizabeth A. Hirshorn,et al.  Localizing interference during naming: Convergent neuroimaging and neuropsychological evidence for the function of Broca's area , 2009, Proceedings of the National Academy of Sciences.