Frequency-based Segregation of Syntactic and Semantic Unification during Online Sentence Level Language Comprehension

During sentence level language comprehension, semantic and syntactic unification are functionally distinct operations. Nevertheless, both recruit roughly the same brain areas (spatially overlapping networks in the left frontotemporal cortex) and happen at the same time (in the first few hundred milliseconds after word onset). We tested the hypothesis that semantic and syntactic unification are segregated by means of neuronal synchronization of the functionally relevant networks in different frequency ranges: gamma (40 Hz and up) for semantic unification and lower beta (10–20 Hz) for syntactic unification. EEG power changes were quantified as participants read either correct sentences, syntactically correct though meaningless sentences (syntactic prose), or sentences that did not contain any syntactic structure (random word lists). Other sentences contained either a semantic anomaly or a syntactic violation at a critical word in the sentence. Larger EEG gamma-band power was observed for semantically coherent than for semantically anomalous sentences. Similarly, beta-band power was larger for syntactically correct sentences than for incorrect ones. These results confirm the existence of a functional dissociation in EEG oscillatory dynamics during sentence level language comprehension that is compatible with the notion of a frequency-based segregation of syntactic and semantic unification.

[1]  Ole Jensen,et al.  Oxford handbook of event-related potential components. , 2011 .

[2]  R. Oostenveld,et al.  Finding Gamma , 2008, Neuron.

[3]  P. Hagoort,et al.  EEG theta and gamma responses to semantic violations in online sentence processing , 2006, Brain and Language.

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

[5]  S. Bookheimer.  Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. , 2002, Annual review of neuroscience.

[6]  P. Mitra,et al.  Analysis of dynamic brain imaging data. , 1998, Biophysical journal.

[7]  Eugenio Rodriguez,et al.  Neural synchrony and the development of cortical networks , 2010, Trends in Cognitive Sciences.

[8]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[9]  F. D. Silva,et al.  EEG and MEG: Relevance to Neuroscience , 2013, Neuron.

[10]  J Gross,et al.  REPRINTS , 1962, The Lancet.

[11]  Ton Dijkstra,et al.  Context-dependent Semantic Processing in the Human Brain: Evidence from Idiom Comprehension , 2013, Journal of Cognitive Neuroscience.

[12]  Sabine Weiss,et al.  Increased neuronal communication accompanying sentence comprehension. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[13]  Giosuè Baggio,et al.  The balance between memory and unification in semantics: A dynamic account of the N400 , 2011 .

[14]  Sabine Weiss,et al.  “Too Many betas do not Spoil the Broth”: The Role of Beta Brain Oscillations in Language Processing , 2012, Front. Psychology.

[15]  Sabine Weiss,et al.  The contribution of EEG coherence to the investigation of language , 2003, Brain and Language.

[16]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[17]  Jan-Mathijs Schoffelen,et al.  A Predictive Coding Perspective on Beta Oscillations during Sentence-Level Language Comprehension , 2016, Front. Hum. Neurosci..

[18]  Markus Werning,et al.  The Oxford Handbook of Compositionality , 2012 .

[19]  G. Kempen,et al.  Syntactic structure assembly in human parsing: a computational model based on competitive inhibition and a lexicalist grammar , 2000, Cognition.

[20]  R. Oostenveld,et al.  Neuronal Dynamics Underlying High- and Low-Frequency EEG Oscillations Contribute Independently to the Human BOLD Signal , 2011, Neuron.

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

[22]  Peter Hagoort,et al.  The neurobiology of language beyond single words. , 2014, Annual review of neuroscience.

[23]  P. Hagoort,et al.  Integration of Word Meaning and World Knowledge in Language Comprehension , 2004, Science.

[24]  Ray Jackendoff,et al.  A Parallel Architecture perspective on language processing , 2007, Brain Research.

[25]  Lucia Melloni,et al.  Brain Oscillations during Spoken Sentence Processing , 2012, Journal of Cognitive Neuroscience.

[26]  Elliot Murphy,et al.  The brain dynamics of linguistic computation , 2015, Front. Psychol..

[27]  Peter Hagoort,et al.  Syntactic Unification Operations Are Reflected in Oscillatory Dynamics during On-line Sentence Comprehension , 2010, Journal of Cognitive Neuroscience.

[28]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[29]  Jayaram Chandrashekar,et al.  Sequential Processing of Lexical, Grammatical, and Phonological Information Within Broca's Area , 2009 .

[30]  Marcel Bastiaansen,et al.  Integration or Predictability? A Further Specification of the Functional Role of Gamma Oscillations in Language Comprehension , 2012, Front. Psychology.

[31]  Nancy Kanwisher,et al.  Neuroimaging of Language: Why Hasn't a Clearer Picture Emerged? , 2009, Lang. Linguistics Compass.

[32]  R. Oostenveld,et al.  I see what you mean: Theta power increases are involved in the retrieval of lexical semantic information , 2008, Brain and Language.

[33]  I. Nelken,et al.  Transient Induced Gamma-Band Response in EEG as a Manifestation of Miniature Saccades , 2008, Neuron.

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

[35]  Peter Hagoort,et al.  MUC (Memory, Unification, Control) and beyond , 2013, Front. Psychol..

[36]  C. Neuper,et al.  Event-related dynamics of brain oscillations , 2006 .

[37]  O. Jensen,et al.  Beyond ERPs: Oscillatory neuronal dynamics , 2012 .

[38]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[39]  Peter Hagoort,et al.  Reflections on the neurobiology of syntax , 2009 .

[40]  Wolf Singer,et al.  Dynamic Formation of Functional Networks by Synchronization , 2011, Neuron.

[41]  Ton Dijkstra,et al.  Theta Responses Are Involved in LexicalSemantic Retrieval during Language Processing , 2005, Journal of Cognitive Neuroscience.

[42]  Peter Hagoort,et al.  So who's "he" anyway? Differential ERP and ERSP effects of referential success, ambiguity and failure during spoken language comprehension , 2004 .