Mapping language with resting‐state functional magnetic resonance imaging: A study on the functional profile of the language network

Resting‐state functional magnetic resonance imaging (rsfMRI) is a promising technique for language mapping that does not require task‐execution. This can be an advantage when language mapping is limited by poor task performance, as is common in clinical settings. Previous studies have shown that language maps extracted with rsfMRI spatially match their task‐based homologs, but no study has yet demonstrated the direct participation of the rsfMRI language network in language processes. This demonstration is critically important because spatial similarity can be influenced by the overlap of domain‐general regions that are recruited during task‐execution. Furthermore, it is unclear which processes are captured by the language network: does it map rather low‐level or high‐level (e.g., syntactic and lexico‐semantic) language processes? We first identified the rsfMRI language network and then investigated task‐based responses within its regions when processing stimuli of increasing linguistic content: symbols, pseudowords, words, pseudosentences and sentences. The language network responded only to language stimuli (not to symbols), and higher linguistic content elicited larger brain responses. The left fronto‐parietal, the default mode, and the dorsal attention networks were examined and yet none showed language involvement. These findings demonstrate for the first time that the language network extracted through rsfMRI is able to map language in the brain, including regions subtending higher‐level syntactic and semantic processes.

[1]  Christian Windischberger,et al.  Toward discovery science of human brain function , 2010, Proceedings of the National Academy of Sciences.

[2]  Nancy Kanwisher,et al.  Neural correlate of the construction of sentence meaning , 2016, Proceedings of the National Academy of Sciences.

[3]  Cathy J. Price,et al.  A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading , 2012, NeuroImage.

[4]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[5]  Evelina Fedorenko,et al.  Domain-General Brain Regions Do Not Track Linguistic Input as Closely as Language-Selective Regions , 2017, The Journal of Neuroscience.

[6]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

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

[8]  Cathy J. Price,et al.  Functional Heterogeneity within the Default Network during Semantic Processing and Speech Production , 2012, Front. Psychology.

[9]  Stefan Sunaert,et al.  Presurgical planning for tumor resectioning , 2006, Journal of magnetic resonance imaging : JMRI.

[10]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[11]  A Aragri,et al.  Does the default-mode functional connectivity of the brain correlate with working-memory performances? , 2009, Archives italiennes de biologie.

[12]  W. K. Simmons,et al.  The Selectivity and Functional Connectivity of the Anterior Temporal Lobes , 2009, Cerebral cortex.

[13]  M. Catani,et al.  A novel frontal pathway underlies verbal fluency in primary progressive aphasia. , 2013, Brain : a journal of neurology.

[14]  S. Jbabdi,et al.  Resting connectivity predicts task activation in pre-surgical populations , 2016, NeuroImage: Clinical.

[15]  Robert Leech,et al.  Domain-general subregions of the medial prefrontal cortex contribute to recovery of language after stroke , 2017, Brain : a journal of neurology.

[16]  Clare Kelly Toward Discovery Science of Human Brain Function: Development , 2010 .

[17]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

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

[19]  Dorothee Saur,et al.  Resting-state functional connectivity: An emerging method for the study of language networks in post-stroke aphasia , 2017, Brain and Cognition.

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

[21]  Paul Hoffman,et al.  The Semantic Network at Work and Rest: Differential Connectivity of Anterior Temporal Lobe Subregions , 2016, The Journal of Neuroscience.

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

[23]  R. Saxe,et al.  Language processing in the occipital cortex of congenitally blind adults , 2011, Proceedings of the National Academy of Sciences.

[24]  Dorothee Saur,et al.  Neuroimaging of stroke recovery from aphasia – Insights into plasticity of the human language network , 2017, NeuroImage.

[25]  Kevin Murphy,et al.  How long to scan? The relationship between fMRI temporal signal to noise ratio and necessary scan duration , 2007, NeuroImage.

[26]  Mikko Sams,et al.  Fronto-parietal network supports context-dependent speech comprehension , 2014, Neuropsychologia.

[27]  José João Almeida,et al.  Procura-PALavras (P-Pal): uma nova medida de frequência lexical do português europeu contemporâneo , 2014 .

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

[29]  Mark W. Woolrich,et al.  Mixture models with adaptive spatial regularization for segmentation with an application to FMRI data , 2005, IEEE Transactions on Medical Imaging.

[30]  Timothy Edward John Behrens,et al.  Task-free MRI predicts individual differences in brain activity during task performance , 2016, Science.

[31]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

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

[33]  Pascale Tremblay,et al.  The frontal aslant tract (FAT) and its role in speech, language and executive function , 2018, Cortex.

[34]  G. Deco,et al.  Emerging concepts for the dynamical organization of resting-state activity in the brain , 2010, Nature Reviews Neuroscience.

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

[36]  Robert Leech,et al.  Overlapping Networks Engaged during Spoken Language Production and Its Cognitive Control , 2014, The Journal of Neuroscience.

[37]  Peter Hagoort,et al.  Shared Syntax in Language Production and Language Comprehension—An fMRI Study , 2011, Cerebral cortex.

[38]  São Luís Castro,et al.  Recognizing emotions in spoken language: A validated set of Portuguese sentences and pseudosentences for research on emotional prosody , 2010, Behavior research methods.

[39]  J. Binder,et al.  A comparison of five fMRI protocols for mapping speech comprehension systems , 2008, Epilepsia.

[40]  J. Binder,et al.  A Parametric Manipulation of Factors Affecting Task-induced Deactivation in Functional Neuroimaging , 2003, Journal of Cognitive Neuroscience.

[41]  Yanmei Tie,et al.  Defining language networks from resting‐state fMRI for surgical planning—a feasibility study , 2014, Human brain mapping.

[42]  Jay J. Pillai,et al.  Relative utility for hemispheric lateralization of different clinical fMRI activation tasks within a comprehensive language paradigm battery in brain tumor patients as assessed by both threshold-dependent and threshold-independent analysis methods , 2011, NeuroImage.

[43]  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.

[44]  N. Kanwisher,et al.  New method for fMRI investigations of language: defining ROIs functionally in individual subjects. , 2010, Journal of neurophysiology.

[45]  S. Thompson-Schill,et al.  Reworking the language network , 2014, Trends in Cognitive Sciences.

[46]  Lauren L. Cloutman,et al.  Exploring distinct default mode and semantic networks using a systematic ICA approach , 2019, Cortex.

[47]  Hermann Ackermann,et al.  The role of the supplementary motor area for speech and language processing , 2016, Neuroscience & Biobehavioral Reviews.

[48]  M. Jenkinson Non-linear registration aka Spatial normalisation , 2007 .

[49]  Martin A Lindquist,et al.  Presurgical brain mapping of the language network in patients with brain tumors using resting‐state fMRI: Comparison with task fMRI , 2016, Human brain mapping.

[50]  Janice Chen,et al.  Dynamic reconfiguration of the default mode network during narrative comprehension , 2016, Nature Communications.

[51]  Karl J. Friston,et al.  Design and analysis of fMRI studies with neurologically impaired patients , 2006, Journal of magnetic resonance imaging : JMRI.

[52]  Susan L. Whitfield-Gabrieli,et al.  Conn: A Functional Connectivity Toolbox for Correlated and Anticorrelated Brain Networks , 2012, Brain Connect..

[53]  J. Kong,et al.  Changes of functional connectivity in the left frontoparietal network following aphasic stroke , 2014, Front. Behav. Neurosci..

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

[55]  Gereon R. Fink,et al.  Dorsal and Ventral Attention Systems , 2014, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[56]  Jessica A. Turner,et al.  Behavioral Interpretations of Intrinsic Connectivity Networks , 2011, Journal of Cognitive Neuroscience.

[57]  Mark D'Esposito,et al.  Focal Brain Lesions to Critical Locations Cause Widespread Disruption of the Modular Organization of the Brain , 2012, Journal of Cognitive Neuroscience.

[58]  William D. Marslen-Wilson,et al.  Left inferior frontal cortex and syntax: function, structure and behaviour in patients with left hemisphere damage , 2011, Brain : a journal of neurology.

[59]  Carl D. Hacker,et al.  A Novel Data-Driven Approach to Preoperative Mapping of Functional Cortex Using Resting-State Functional Magnetic Resonance Imaging , 2013, Neurosurgery.

[60]  Evelina Fedorenko The role of domain-general cognitive control in language comprehension , 2014, Front. Psychol..

[61]  B. Biswal,et al.  The resting brain: unconstrained yet reliable. , 2009, Cerebral cortex.

[62]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[63]  Stephen M. Wilson,et al.  Validity and reliability of four language mapping paradigms , 2016, NeuroImage: Clinical.

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

[65]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[66]  A. Content,et al.  BACS: The Brussels Artificial Character Sets for studies in cognitive psychology and neuroscience , 2017, Behavior Research Methods.

[67]  Jeffrey R. Binder,et al.  Some neurophysiological constraints on models of word naming , 2005, NeuroImage.

[68]  Nancy Kanwisher,et al.  Language-Selective and Domain-General Regions Lie Side by Side within Broca’s Area , 2012, Current Biology.

[69]  Susan Bookheimer,et al.  Pre-Surgical Language Mapping with Functional Magnetic Resonance Imaging , 2007, Neuropsychology Review.

[70]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[71]  Jeffrey N. Rouder,et al.  Bayesian inference for psychology. Part II: Example applications with JASP , 2017, Psychonomic Bulletin & Review.

[72]  A. Turken,et al.  The Neural Architecture of the Language Comprehension Network: Converging Evidence from Lesion and Connectivity Analyses , 2011, Front. Syst. Neurosci..

[73]  S. Rombouts,et al.  Within-subject reproducibility of visual activation patterns with functional magnetic resonance imaging using multislice echo planar imaging. , 1998, Magnetic resonance imaging.

[74]  Nancy Kanwisher,et al.  Broad domain generality in focal regions of frontal and parietal cortex , 2013, Proceedings of the National Academy of Sciences.

[75]  Alberto Llera,et al.  ICA-AROMA: A robust ICA-based strategy for removing motion artifacts from fMRI data , 2015, NeuroImage.

[76]  Thomas E. Nichols,et al.  Power calculation for group fMRI studies accounting for arbitrary design and temporal autocorrelation , 2008, NeuroImage.

[77]  B. Thomas,et al.  Resting-State Seed-Based Analysis: An Alternative to Task-Based Language fMRI and Its Laterality Index , 2017, American Journal of Neuroradiology.

[78]  Ronald Peeters,et al.  Resting-State Functional Magnetic Resonance Imaging for Language Preoperative Planning , 2016, Front. Hum. Neurosci..

[79]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[80]  Pascale Tremblay,et al.  Broca and Wernicke are dead, or moving past the classic model of language neurobiology , 2016, Brain and Language.

[81]  M. Greicius,et al.  Decoding subject-driven cognitive states with whole-brain connectivity patterns. , 2012, Cerebral cortex.

[82]  Gina F. Humphreys,et al.  Fusion and Fission of Cognitive Functions in the Human Parietal Cortex , 2014, Cerebral cortex.

[83]  César F. Lima,et al.  Roles of Supplementary Motor Areas in Auditory Processing and Auditory Imagery , 2016, Trends in Neurosciences.

[84]  Stephen M. Smith,et al.  Probabilistic independent component analysis for functional magnetic resonance imaging , 2004, IEEE Transactions on Medical Imaging.

[85]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[86]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[87]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[88]  Paulo Branco,et al.  Temporal reliability of ultra-high field resting-state MRI for single-subject sensorimotor and language mapping , 2016, NeuroImage.

[89]  David J. Webb,et al.  Emerging Concepts , 2009 .

[90]  Ernst Nennig,et al.  Localizing and lateralizing language in patients with brain tumors: feasibility of routine preoperative functional MR imaging in 81 consecutive patients. , 2007, Radiology.