Effective connectivity of cortical and subcortical regions during unification of sentence structure

In a recent fMRI study we showed that left posterior middle temporal gyrus (LpMTG) subserves the retrieval of a word's lexical-syntactic properties from the mental lexicon (long-term memory), while left posterior inferior frontal gyrus (LpIFG) is involved in unifying (on-line integration of) this information into a sentence structure (Snijders et al., 2009). In addition, the right IFG, right MTG, and the right striatum were involved in the unification process. Here we report results from a psychophysical interactions (PPI) analysis in which we investigated the effective connectivity between LpIFG and LpMTG during unification, and how the right hemisphere areas and the striatum are functionally connected to the unification network. LpIFG and LpMTG both showed enhanced connectivity during the unification process with a region slightly superior to our previously reported LpMTG. Right IFG better predicted right temporal activity when unification processes were more strongly engaged, just as LpIFG better predicted left temporal activity. Furthermore, the striatum showed enhanced coupling to LpIFG and LpMTG during unification. We conclude that bilateral inferior frontal and posterior temporal regions are functionally connected during sentence-level unification. Cortico-subcortical connectivity patterns suggest cooperation between inferior frontal and striatal regions in performing unification operations on lexical-syntactic representations retrieved from LpMTG.

[1]  Peter Hagoort,et al.  UvA-DARE (Digital Academic Repository) Unification of speaker and meaning in language comprehension: an fMRI study , 2022 .

[2]  A. Friederici,et al.  Why the P600 is not just a P300: the role of the basal ganglia , 2003, Clinical Neurophysiology.

[3]  T. Parrish,et al.  Argument structure effects in action verb naming in static and dynamic conditions , 2009, Journal of Neurolinguistics.

[4]  A. Wingfield,et al.  Neural processing during older adults' comprehension of spoken sentences: age differences in resource allocation and connectivity. , 2010, Cerebral cortex.

[5]  P. McGuire,et al.  Engagement of right temporal cortex during processing of linguistic context , 2001, Neuropsychologia.

[6]  Michael J. Frank,et al.  Dynamic Dopamine Modulation in the Basal Ganglia: A Neurocomputational Account of Cognitive Deficits in Medicated and Nonmedicated Parkinsonism , 2005, Journal of Cognitive Neuroscience.

[7]  Michael J. Frank,et al.  Interactions between frontal cortex and basal ganglia in working memory: A computational model , 2001, Cognitive, affective & behavioral neuroscience.

[8]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[9]  Bruce D. McCandliss,et al.  The visual word form area: expertise for reading in the fusiform gyrus , 2003, Trends in Cognitive Sciences.

[10]  Y. Miyashita,et al.  Top-down signal from prefrontal cortex in executive control of memory retrieval , 1999, Nature.

[11]  P. Skudlarski,et al.  Detection of functional connectivity using temporal correlations in MR images , 2002, Human brain mapping.

[12]  J. Gee,et al.  Neural representation of verb meaning: An fMRI study , 2002, Human brain mapping.

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

[14]  Thomas E. Hazy,et al.  Towards an executive without a homunculus: computational models of the prefrontal cortex/basal ganglia system , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[15]  T. Klingberg,et al.  Prefrontal cortex and basal ganglia control access to working memory , 2008, Nature Neuroscience.

[16]  Mark W. Greenlee,et al.  Evidence of fronto-temporal interactions for strategic inference processes during language comprehension , 2008, NeuroImage.

[17]  M. Just,et al.  The neural bases of sentence comprehension: a fMRI examination of syntactic and lexical processing. , 2001, Cerebral cortex.

[18]  Karl J. Friston,et al.  Dynamic causal modeling , 2010, Scholarpedia.

[19]  Karl J. Friston,et al.  Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution , 2003, NeuroImage.

[20]  Mark D'Esposito,et al.  Searching for “the Top” in Top-Down Control , 2005, Neuron.

[22]  Karl Magnus Petersson,et al.  Artificial syntactic violations activate Broca's region , 2004 .

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

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

[25]  Karl J. Friston,et al.  PHRENOLOGY : What Can Neuroimaging Tell Us About Distributed Circuitry ? , 2005 .

[26]  A. Friederici,et al.  The role of the posterior superior temporal cortex in sentence comprehension , 2009, Neuroreport.

[27]  Shari R. Baum,et al.  Hemispheric contributions to lexical ambiguity resolution in a discourse context: Evidence from individuals with unilateral left and right hemisphere lesions , 2005, Brain and Cognition.

[28]  C. Curtis,et al.  Persistent activity in the prefrontal cortex during working memory , 2003, Trends in Cognitive Sciences.

[29]  S. Thompson-Schill,et al.  Semantic adaptation and competition during word comprehension. , 2008, Cerebral cortex.

[30]  J. Fuster Prefrontal Cortex , 2018 .

[31]  Roel M. Willems,et al.  Seeing and Hearing Meaning: ERP and fMRI Evidence of Word versus Picture Integration into a Sentence Context , 2008, Journal of Cognitive Neuroscience.

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

[33]  Robert T. Knight,et al.  Superior Temporal SulcusIt's My Area: Or Is It? , 2008, Journal of Cognitive Neuroscience.

[34]  R. Jackendoff Foundations of Language: Brain, Meaning, Grammar, Evolution , 2002 .

[35]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[36]  Matthew H. Davis,et al.  Dissociating speech perception and comprehension at reduced levels of awareness , 2007, Proceedings of the National Academy of Sciences.

[37]  R. Buckner,et al.  Common Prefrontal Regions Coactivate with Dissociable Posterior Regions during Controlled Semantic and Phonological Tasks , 2002, Neuron.

[38]  Alfonso Caramazza,et al.  Cortical signatures of noun and verb production , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Michael J. Frank,et al.  Making Working Memory Work: A Computational Model of Learning in the Prefrontal Cortex and Basal Ganglia , 2006, Neural Computation.

[40]  Noriaki Yahata,et al.  Selective enhancement of functional connectivity in the left prefrontal cortex during sentence processing , 2003, NeuroImage.

[41]  W. Marslen-Wilson Functional parallelism in spoken word-recognition , 1987, Cognition.

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

[43]  C. Fiebach,et al.  The role of left inferior frontal and superior temporal cortex in sentence comprehension: localizing syntactic and semantic processes. , 2003, Cerebral cortex.

[44]  A. Dale,et al.  Distinct Patterns of Neural Modulation during the Processing of Conceptual and Syntactic Anomalies , 2003, Journal of Cognitive Neuroscience.

[45]  G. Paxinos,et al.  Atlas of the Human Brain , 2000 .

[46]  Colin Humphries,et al.  Time course of semantic processes during sentence comprehension: An fMRI study , 2007, NeuroImage.

[47]  Z. Harris,et al.  Foundations of language , 1941 .

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

[49]  Remco J. Renken,et al.  Semantic ambiguity processing in sentence context: Evidence from event-related fMRI , 2007, NeuroImage.

[50]  Terry M. Peters,et al.  3D statistical neuroanatomical models from 305 MRI volumes , 1993, 1993 IEEE Conference Record Nuclear Science Symposium and Medical Imaging Conference.

[51]  Peter Hagoort,et al.  When Elephants Fly: Differential Sensitivity of Right and Left Inferior Frontal Gyri to Discourse and World Knowledge , 2009, Journal of Cognitive Neuroscience.

[52]  Matthew H. Davis,et al.  The neural mechanisms of speech comprehension: fMRI studies of semantic ambiguity. , 2005, Cerebral cortex.

[53]  J. Stevenson,et al.  Human language and our reptilian brain: The subcortical bases of speech, syntax, and thought , 2001 .

[54]  Roel M. Willems,et al.  Differential roles for left inferior frontal and superior temporal cortex in multimodal integration of action and language , 2009, NeuroImage.

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

[56]  D. Shankweiler,et al.  An Event-related Neuroimaging Study Distinguishing Form and Content in Sentence Processing , 2000, Journal of Cognitive Neuroscience.

[57]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[58]  Karl J. Friston,et al.  Detecting Activations in PET and fMRI: Levels of Inference and Power , 1996, NeuroImage.

[59]  Christine Chiarello,et al.  Sentence context and lexical ambiguity resolution by the two hemispheres , 1998, Neuropsychologia.

[60]  Noam Chomsky,et al.  The Minimalist Program , 1992 .

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

[62]  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.

[63]  Roshan Cools,et al.  Role of Dopamine in the Motivational and Cognitive Control of Behavior , 2008, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[64]  Roel M. Willems,et al.  When language meets action: the neural integration of gesture and speech. , 2007, Cerebral cortex.

[65]  C. Fiebach,et al.  Modulation of Inferotemporal Cortex Activation during Verbal Working Memory Maintenance , 2006, Neuron.

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

[67]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[68]  Michael A. Kraut,et al.  Neural Basis of Semantic Memory: Insights from Electrophysiology , 2007 .

[69]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[70]  J. Kaiser,et al.  Object Familiarity and Semantic Congruency Modulate Responses in Cortical Audiovisual Integration Areas , 2007, The Journal of Neuroscience.

[71]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[72]  Caroline F. Zink,et al.  Human striatal activation reflects degree of stimulus saliency , 2006, NeuroImage.

[73]  Anton Nijholt,et al.  Computational Linguistics in the Netherlands 2001 , 2002 .

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

[75]  W. Schultz,et al.  Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[76]  Karl J. Friston,et al.  Behavioral / Systems / Cognitive Striatal Prediction Error Modulates Cortical Coupling , 2010 .

[77]  Bruce Crosson,et al.  Neural Basis of Semantic Memory: Role of the basal ganglia in language and semantics: supporting cast , 2007 .

[78]  Marcel Adam Just,et al.  Individual Differences in Sentence Comprehension: A Functional Magnetic Resonance Imaging Investigation of Syntactic and Lexical Processing Demands , 2007, Journal of Cognitive Neuroscience.

[79]  J. Mink THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS , 1996, Progress in Neurobiology.

[80]  M. Jung-Beeman Bilateral brain processes for comprehending natural language , 2005, Trends in Cognitive Sciences.

[81]  W. Levelt Accessing words in speech production: Stages, processes and representations , 1992, Cognition.

[82]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[83]  Evelyn C. Ferstl,et al.  The extended language network: A meta‐analysis of neuroimaging studies on text comprehension , 2008, Human brain mapping.

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

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

[86]  Peter Dayan,et al.  Simple Substrates for Complex Cognition , 2008, Front. Neurosci..

[87]  Lorraine K Tyler,et al.  Fronto-temporal brain systems supporting spoken language comprehension , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[88]  Richard S. J. Frackowiak,et al.  Noun and verb retrieval by normal subjects. Studies with PET. , 1996, Brain : a journal of neurology.

[89]  Gertjan van Noord,et al.  The Alpino Dependency Treebank , 2001, CLIN.

[90]  J. Fuster The Prefrontal Cortex—An Update Time Is of the Essence , 2001, Neuron.

[91]  M. Ullman Contributions of memory circuits to language: the declarative/procedural model , 2004, Cognition.

[92]  C. Fiebach,et al.  Revisiting the role of Broca's area in sentence processing: Syntactic integration versus syntactic working memory , 2005, Human brain mapping.

[93]  Boris S. Gutkin,et al.  Dopamine modulation in the basal ganglia locks the gate to working memory , 2006, Journal of Computational Neuroscience.

[94]  Matthew H. Davis,et al.  Neural responses to morphological, syntactic, and semantic properties of single words: An fMRI study , 2004, Brain and Language.

[95]  Gerard Kempen,et al.  The Unification Space implemented as a localist neural net: predictions and error-tolerance in a constraint-based parser , 2009, Cognitive Neurodynamics.