Exploring the temporal dynamics of speech production with EEG and group ICA

Speech production is a complex skill whose neural implementation relies on a large number of different regions in the brain. How neural activity in these different regions varies as a function of time during the production of speech remains poorly understood. Previous MEG studies on this topic have concluded that activity proceeds from posterior to anterior regions of the brain in a sequential manner. Here we tested this claim using the EEG technique. Specifically, participants performed a picture naming task while their naming latencies and scalp potentials were recorded. We performed group temporal Independent Component Analysis (group tICA) to obtain temporally independent component timecourses and their corresponding topographic maps. We identified fifteen components whose estimated neural sources were located in various areas of the brain. The trial-by-trial component timecourses were predictive of the naming latency, implying their involvement in the task. Crucially, we computed the degree of concurrent activity of each component timecourse to test whether activity was sequential or parallel. Our results revealed that these fifteen distinct neural sources exhibit largely concurrent activity during speech production. These results suggest that speech production relies on neural activity that takes place in parallel networks of distributed neural sources.

[1]  Arnaud Delorme,et al.  Grand average ERP-image plotting and statistics: A method for comparing variability in event-related single-trial EEG activities across subjects and conditions , 2015, Journal of Neuroscience Methods.

[2]  Pierre Comon Independent component analysis - a new concept? signal processing , 1994 .

[3]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[4]  Jack J. Lin,et al.  Direct brain recordings reveal hippocampal rhythm underpinnings of language processing , 2016, Proceedings of the National Academy of Sciences.

[5]  Peter Indefrey,et al.  On putative shortcomings and dangerous future avenues: response to Strijkers & Costa , 2016 .

[6]  Thomas E. Nichols,et al.  Functional connectomics from resting-state fMRI , 2013, Trends in Cognitive Sciences.

[7]  S. Bressler,et al.  Synchronized activity in prefrontal cortex during anticipation of visuomotor processing , 2002, Neuroreport.

[8]  Terrence J. Sejnowski,et al.  Enhanced detection of artifacts in EEG data using higher-order statistics and independent component analysis , 2007, NeuroImage.

[9]  F. Pulvermüller,et al.  Early Parallel Activation of Semantics and Phonology in Picture Naming: Evidence from a Multiple Linear Regression MEG Study , 2014, Cerebral cortex.

[10]  Niels Janssen,et al.  The Dynamics of Speech Motor Control Revealed with Time-Resolved fMRI. , 2020, Cerebral cortex.

[11]  Borís Burle,et al.  Response-Locked Brain Dynamics of Word Production , 2013, PloS one.

[12]  R Salmelin,et al.  Comparing MEG and fMRI views to naming actions and objects , 2009, NeuroImage.

[13]  Riitta Salmelin,et al.  Accessing newly learned names and meanings in the native language , 2009, Human brain mapping.

[14]  D. Guthrie,et al.  Significance testing of difference potentials. , 1991, Psychophysiology.

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

[16]  Natasa Kovacevic,et al.  Groupwise independent component decomposition of EEG data and partial least square analysis , 2007, NeuroImage.

[17]  B. Horwitz,et al.  Laryngeal Motor Cortex and Control of Speech in Humans , 2011, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[18]  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.

[19]  U. Jürgens Neural pathways underlying vocal control , 2002, Neuroscience & Biobehavioral Reviews.

[20]  Pierre Comon,et al.  Independent component analysis, A new concept? , 1994, Signal Process..

[21]  Klaus-Robert Müller,et al.  On the influence of high-pass filtering on ICA-based artifact reduction in EEG-ERP , 2015, 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[22]  Keith Johnson,et al.  Encoding of Articulatory Kinematic Trajectories in Human Speech Sensorimotor Cortex , 2018, Neuron.

[23]  Albert Costa,et al.  The cortical dynamics of speaking: present shortcomings and future avenues , 2016 .

[24]  S. Bressler Large-scale cortical networks and cognition , 1995, Brain Research Reviews.

[25]  C. Berrou,et al.  Dynamic reorganization of functional brain networks during picture naming , 2015, Cortex.

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

[27]  Albert Costa,et al.  The time course of word retrieval revealed by event-related brain potentials during overt speech , 2009, Proceedings of the National Academy of Sciences.

[28]  D. Tucker,et al.  EEG source localization: Sensor density and head surface coverage , 2015, Journal of Neuroscience Methods.

[29]  R. Hari,et al.  Dynamics of brain activation during picture naming , 1994, Nature.

[30]  Daniel Herron,et al.  A new on-line resource for psycholinguistic studies. , 2004, Journal of memory and language.

[31]  J. Kalaska,et al.  Neural mechanisms for interacting with a world full of action choices. , 2010, Annual review of neuroscience.

[32]  Don M. Tucker,et al.  Sensor density and head surface coverage in EEG source localization , 2014, 2014 IEEE 11th International Symposium on Biomedical Imaging (ISBI).

[33]  G A Ojemann,et al.  Language-related potentials specific to human language cortex. , 1981, Science.

[34]  Todd C. Handy,et al.  Event-related potentials : a methods handbook , 2005 .

[35]  R. Oostenveld,et al.  Independent EEG Sources Are Dipolar , 2012, PloS one.

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

[37]  Riitta Salmelin,et al.  Naming actions and objects: cortical dynamics in healthy adults and in an anomic patient with a dissociation in action/object naming , 2003, NeuroImage.

[38]  W. Glaser Picture naming , 1992, Cognition.

[39]  S. Hillyard,et al.  Cortical sources of the early components of the visual evoked potential , 2002, Human brain mapping.

[40]  S. Makeig,et al.  Mining event-related brain dynamics , 2004, Trends in Cognitive Sciences.

[41]  Riitta Salmelin,et al.  Cortical dynamics of visual/semantic vs. phonological analysis in picture confrontation , 2006, NeuroImage.

[42]  S. Bressler,et al.  Large-scale visuomotor integration in the cerebral cortex. , 2007, Cerebral cortex.

[43]  M. Erb,et al.  fMRI reveals two distinct cerebral networks subserving speech motor control , 2005, Neurology.

[44]  Lüder Deecke,et al.  Brain potential changes in voluntary and passive movements in humans: readiness potential and reafferent potentials , 2016, Pflügers Archiv - European Journal of Physiology.

[45]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[46]  E. Fetz Movement control: Are movement parameters recognizably coded in the activity of single neurons? , 1992 .

[47]  Athanassios Protopapas,et al.  Check Vocal: A program to facilitate checking the accuracy and response time of vocal responses from DMDX , 2007, Behavior research methods.

[48]  T. Sejnowski,et al.  Electroencephalographic Brain Dynamics Following Manually Responded Visual Targets , 2004, PLoS biology.

[49]  Aapo Hyvärinen,et al.  Fast and robust fixed-point algorithms for independent component analysis , 1999, IEEE Trans. Neural Networks.

[50]  Werner Sommer,et al.  Does phonological encoding in speech production always follow the retrieval of semantic knowledge? Electrophysiological evidence for parallel processing. , 2003, Brain research. Cognitive brain research.

[51]  F.-Xavier Alario,et al.  On the cortical dynamics of word production: a review of the MEG evidence , 2016 .

[52]  Niels Janssen,et al.  Tracking the Time Course of Competition During Word Production: Evidence for a Post-Retrieval Mechanism of Conflict Resolution. , 2015, Cerebral cortex.

[53]  Erich Schröger,et al.  Digital filter design for electrophysiological data – a practical approach , 2015, Journal of Neuroscience Methods.

[54]  Alan C. Evans,et al.  The Neural Substrate of Picture Naming , 1999, Journal of Cognitive Neuroscience.

[55]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[56]  Arnaud Delorme,et al.  Applying dimension reduction to EEG data by Principal Component Analysis reduces the quality of its subsequent Independent Component decomposition , 2018, NeuroImage.

[57]  C. Joyce,et al.  Automatic removal of eye movement and blink artifacts from EEG data using blind component separation. , 2004, Psychophysiology.

[58]  J Vieth,et al.  New approach to localize speech relevant brain areas and hemispheric dominance using spatially filtered magnetoencephalography , 2001, Human brain mapping.

[59]  Robert Leech,et al.  The contribution of the inferior parietal cortex to spoken language production , 2012, Brain and Language.

[60]  Sharon L. Thompson-Schill,et al.  Functional Neuroimaging Can Support Causal Claims about Brain Function , 2010, Journal of Cognitive Neuroscience.

[61]  Emmanuel Mellet,et al.  Picture naming without Broca's and Wernicke's area , 2000, Neuroreport.

[62]  T. Sejnowski,et al.  Dynamic Brain Sources of Visual Evoked Responses , 2002, Science.

[63]  S. Luck,et al.  How inappropriate high-pass filters can produce artifactual effects and incorrect conclusions in ERP studies of language and cognition. , 2015, Psychophysiology.

[64]  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.

[65]  Marina Laganaro,et al.  Spatio-temporal Dynamics of Referential and Inferential Naming: Different Brain and Cognitive Operations to Lexical Selection , 2017, Brain Topography.

[66]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[67]  E. Schröger,et al.  High-pass filters and baseline correction in M/EEG analysis. Commentary on: “How inappropriate high-pass filters can produce artefacts and incorrect conclusions in ERP studies of language and cognition” , 2016, Journal of Neuroscience Methods.

[68]  C. Beckmann,et al.  Using Dual Regression to Investigate Network Shape and Amplitude in Functional Connectivity Analyses , 2017, Front. Neurosci..

[69]  Andrea Krott,et al.  Removing speech artifacts from electroencephalographic recordings during overt picture naming , 2015, NeuroImage.