Cortical theta wanes for language

The role of low frequency oscillations in language areas is not yet understood. Using ECoG in six human subjects, we studied whether different language regions show prominent power changes in a specific rhythm, in similar manner as the alpha rhythm shows the most prominent power changes in visual areas. Broca's area and temporal language areas were localized in individual subjects using fMRI. In these areas, the theta rhythm showed the most pronounced power changes and theta power decreased significantly during verb generation. To better understand the role of this language-related theta decrease, we then studied the interaction between low frequencies and local neuronal activity reflected in high frequencies. Amplitude-amplitude correlations showed that theta power correlated negatively with high frequency activity, specifically across verb generation trials. Phase-amplitude coupling showed that during control trials, high frequency power was coupled to theta phase, but this coupling decreased significantly during verb generation trials. These results suggest a dynamic interaction between the neuronal mechanisms underlying the theta rhythm and local neuronal activity in language areas. As visual areas show a pronounced alpha rhythm that may reflect pulsed inhibition, language regions show a pronounced theta rhythm with highly similar features.

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

[2]  O Jensen,et al.  An Oscillatory Short-Term Memory Buffer Model Can Account for Data on the Sternberg Task , 1998, The Journal of Neuroscience.

[3]  J. Maunsell,et al.  Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex , 2011, PLoS biology.

[4]  J E Lisman,et al.  Theta oscillations in human cortex during a working-memory task: evidence for local generators. , 2006, Journal of neurophysiology.

[5]  Charles E. Schroeder,et al.  Dual Mechanism of Neuronal Ensemble Inhibition in Primary Auditory Cortex , 2011, Neuron.

[6]  Partha P. Mitra,et al.  Observed Brain Dynamics , 2007 .

[7]  Jeffrey G. Ojemann,et al.  Power-Law Scaling in the Brain Surface Electric Potential , 2009, PLoS Comput. Biol..

[8]  Eric Leuthardt,et al.  Spatiotemporal dynamics of electrocorticographic high gamma activity during overt and covert word repetition , 2011, NeuroImage.

[9]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[10]  D. Poeppel,et al.  Phase Patterns of Neuronal Responses Reliably Discriminate Speech in Human Auditory Cortex , 2007, Neuron.

[11]  Arne D. Ekstrom,et al.  Correlation between BOLD fMRI and theta-band local field potentials in the human hippocampal area. , 2009, Journal of neurophysiology.

[12]  Robert Oostenveld,et al.  Trial-by-trial coupling between EEG and BOLD identifies networks related to alpha and theta EEG power increases during working memory maintenance , 2009, NeuroImage.

[13]  Timothy M. Ellmore,et al.  Frequency-specific electrocorticographic correlates of working memory delay period fMRI activity , 2011, NeuroImage.

[14]  Richard S. J. Frackowiak,et al.  Endogenous Cortical Rhythms Determine Cerebral Specialization for Speech Perception and Production , 2007, Neuron.

[15]  B. Staresina,et al.  Medial Temporal Theta/Alpha Power Enhancement Precedes Successful Memory Encoding: Evidence Based on Intracranial EEG , 2011, The Journal of Neuroscience.

[16]  N. Barbaro,et al.  Spatiotemporal Dynamics of Word Processing in the Human Brain , 2007, Front. Neurosci..

[17]  M. Whittington,et al.  A Novel Network of Multipolar Bursting Interneurons Generates Theta Frequency Oscillations in Neocortex , 2003, Neuron.

[18]  Guy Marchal,et al.  Multimodality image registration by maximization of mutual information , 1997, IEEE Transactions on Medical Imaging.

[19]  Nick F. Ramsey,et al.  Human Motor Cortical Activity Is Selectively Phase-Entrained on Underlying Rhythms , 2012, PLoS Comput. Biol..

[20]  G. J. M. Rutten,et al.  fMRI-Determined Language Lateralization in Patients with Unilateral or Mixed Language Dominance According to the Wada Test , 2002, NeuroImage.

[21]  Eric Halgren,et al.  Sequential Processing of Lexical, Grammatical, and Phonological Information Within Broca’s Area , 2009, Science.

[22]  C. Schroeder,et al.  Low-frequency neuronal oscillations as instruments of sensory selection , 2009, Trends in Neurosciences.

[23]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[24]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[25]  Nick F. Ramsey,et al.  Automated electrocorticographic electrode localization on individually rendered brain surfaces , 2010, Journal of Neuroscience Methods.

[26]  N. F. Ramsey,et al.  Reproducibility of fMRI-Determined Language Lateralization in Individual Subjects , 2002, Brain and Language.

[27]  Christopher J. Aura,et al.  Divergence of fMRI and neural signals in V1 during perceptual suppression in the awake monkey , 2008, Nature Neuroscience.

[28]  G A Ojemann,et al.  Electrocorticographic (ECoG) correlates of language. I. Desynchronization in temporal language cortex during object naming. , 1989, Electroencephalography and clinical neurophysiology.

[29]  Arne D. Ekstrom,et al.  Human hippocampal theta activity during virtual navigation , 2005, Hippocampus.

[30]  Edward K. Vogel,et al.  Dynamic Neuroplasticity after Human Prefrontal Cortex Damage , 2010, Neuron.

[31]  Krish D. Singh,et al.  Functional decoupling of BOLD and gamma‐band amplitudes in human primary visual cortex , 2009, Human brain mapping.

[32]  N. Ramsey,et al.  Neurophysiologic correlates of fMRI in human motor cortex , 2012, Human brain mapping.

[33]  S. Francis,et al.  Theta power during encoding predicts subsequent‐memory performance and default mode network deactivation , 2013, Human brain mapping.

[34]  G. Buzsáki,et al.  A neural coding scheme formed by the combined function of gamma and theta oscillations. , 2008, Schizophrenia bulletin.

[35]  I. Fried,et al.  Coupling Between Neuronal Firing, Field Potentials, and fMRI in Human Auditory Cortex , 2005, Science.

[36]  Rajesh P. N. Rao,et al.  Dynamic Modulation of Local Population Activity by Rhythm Phase in Human Occipital Cortex During a Visual Search Task , 2010, Front. Hum. Neurosci..

[37]  Yevgeniy B. Sirotin,et al.  Anticipatory haemodynamic signals in sensory cortex not predicted by local neuronal activity. , 2009, Nature.

[38]  A. Walden,et al.  Spectral analysis for physical applications : multitaper and conventional univariate techniques , 1996 .

[39]  H. Noordmans,et al.  Development of a functional magnetic resonance imaging protocol for intraoperative localization of critical temporoparietal language areas , 2002, Annals of neurology.

[40]  Yoko Yamaguchi,et al.  A long-range cortical network emerging with theta oscillation in a mental task , 2004, Neuroreport.

[41]  Jeremy R. Manning,et al.  Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans , 2009, The Journal of Neuroscience.

[42]  Erno J. Hermans,et al.  Enhanced sensitivity with fast three‐dimensional blood‐oxygen‐level‐dependent functional MRI: comparison of SENSE–PRESTO and 2D‐EPI at 3 T , 2008, NMR in biomedicine.

[43]  B. Crosson.  Subcortical functions in language: A working model , 1985, Brain and Language.

[44]  Robert T. Knight,et al.  Spatiotemporal imaging of cortical activation during verb generation and picture naming , 2010, NeuroImage.

[45]  T A Yousry,et al.  Preoperative activation and intraoperative stimulation of language-related areas in patients with glioma. , 1997, Neurosurgery.

[46]  Dennis J. McFarland,et al.  Electroencephalographic(EEG)-based communication: EEG control versus system performance in humans , 2003, Neuroscience Letters.

[47]  O. Jensen,et al.  Frontal theta activity in humans increases with memory load in a working memory task , 2002, The European journal of neuroscience.

[48]  G A Ojemann,et al.  Individual variability in cortical localization of language. , 1979, Journal of neurosurgery.

[49]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[50]  Nicole C. Swann,et al.  Deep Brain Stimulation of the Subthalamic Nucleus Alters the Cortical Profile of Response Inhibition in the Beta Frequency Band: A Scalp EEG Study in Parkinson's Disease , 2011, The Journal of Neuroscience.

[51]  O. Bertrand,et al.  Relationship between task‐related gamma oscillations and BOLD signal: New insights from combined fMRI and intracranial EEG , 2007, Human brain mapping.

[52]  Nick F Ramsey,et al.  Discrepant findings for Wada test and functional magnetic resonance imaging with regard to language function: use of electrocortical stimulation mapping to confirm results. Case report. , 2005, Journal of neurosurgery.

[53]  C. Schroeder,et al.  Neuronal Mechanisms and Attentional Modulation of Corticothalamic Alpha Oscillations , 2011, The Journal of Neuroscience.

[54]  O. Jensen,et al.  Prestimulus alpha and mu activity predicts failure to inhibit motor responses , 2009, Human brain mapping.