Characteristic profiles of high gamma activity and blood oxygenation level-dependent responses in various language areas

High gamma activity (HGA) has been shown to be positively correlated with blood oxygenation level-dependent (BOLD) responses in the primary cortices with simple tasks. It is, however, an open question whether the correlation is simply applied to the association areas related to higher cognitive functions. The aim of this study is to investigate quantitative correlation between HGA and BOLD and their spatial and temporal profiles during semantic processing. Thirteen patients with intractable epilepsy underwent fMRI and electrocorticography (ECoG) with a word interpretation task to evoke language-related responses. Percent signal change of BOLD was calculated at each site of ECoG electrode, which has power amplification of high gamma band (60-120 Hz) activity. We transformed locations of individual electrodes and brains to a universal coordination using SPM8 and made the quantitative comparisons on a template brain. HGAs were increased in several language-related areas such as the inferior frontal and middle temporal gyri and were positively correlated with BOLD responses. The most striking finding was different temporal dynamics of HGAs in the different brain regions. Whereas the frontal lobe showed longer-lasting HGA, the HGA-intensity on the temporal lobe quickly declined. The different temporal dynamics of HGA might explain why routine language-fMRI hardly detected BOLD in the temporal lobe. This study clarified different neural oscillation and BOLD response in various brain regions during semantic processing and will facilitate practical utilization of fMRI for evaluating higher-order cognitive functions not only in basic neuroscience, but also in clinical practice.

[1]  Jessica A. Cardin,et al.  Driving fast-spiking cells induces gamma rhythm and controls sensory responses , 2009, Nature.

[2]  G. Ojemann,et al.  Neuronal correlates of functional magnetic resonance imaging in human temporal cortex , 2009, Brain : a journal of neurology.

[3]  A. Bizzi,et al.  Presurgical functional MR imaging of language and motor functions: validation with intraoperative electrocortical mapping. , 2008, Radiology.

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

[5]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

[6]  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.

[7]  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.

[8]  Roger D. Traub,et al.  Simulation of Gamma Rhythms in Networks of Interneurons and Pyramidal Cells , 1997, Journal of Computational Neuroscience.

[9]  U Noppeney,et al.  The neural areas that control the retrieval and selection of semantics , 2004, Neuropsychologia.

[10]  Arne D. Ekstrom,et al.  How and when the fMRI BOLD signal relates to underlying neural activity: The danger in dissociation , 2010, Brain Research Reviews.

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

[12]  D. V. von Cramon,et al.  Temporal properties of the hemodynamic response in functional MRI , 1999, Human brain mapping.

[13]  Leslie G. Ungerleider,et al.  Discrete Cortical Regions Associated with Knowledge of Color and Knowledge of Action , 1995, Science.

[14]  W. Singer,et al.  Hemodynamic Signals Correlate Tightly with Synchronized Gamma Oscillations , 2005, Science.

[15]  Eishi Asano,et al.  Gamma-oscillations modulated by picture naming and word reading: Intracranial recording in epileptic patients , 2011, Clinical Neurophysiology.

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

[17]  R. E. Greenblatt,et al.  Inferring spatiotemporal network patterns from intracranial EEG data , 2010, Clinical Neurophysiology.

[18]  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.

[19]  D. Attwell,et al.  The neural basis of functional brain imaging signals , 2002, Trends in Neurosciences.

[20]  I. Fried,et al.  Coupling between Neuronal Firing Rate, Gamma LFP, and BOLD fMRI Is Related to Interneuronal Correlations , 2007, Current Biology.

[21]  N Kopell,et al.  Gap Junctions between Interneuron Dendrites Can Enhance Synchrony of Gamma Oscillations in Distributed Networks , 2001, The Journal of Neuroscience.

[22]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[23]  N. Tandon Expressive and receptive language areas determined by a non-invasive reliable method using functional magnetic resonance imaging and magnetoencephalography , 2008 .

[24]  Karl J. Friston,et al.  Regionally Specific Sensitivity Differences in fMRI and PET: Where Do They Come From? , 2000, NeuroImage.

[25]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[26]  G. Buzsáki,et al.  Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model , 1996, The Journal of Neuroscience.

[27]  Miles A. Whittington,et al.  Impaired Electrical Signaling Disrupts Gamma Frequency Oscillations in Connexin 36-Deficient Mice , 2001, Neuron.

[28]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[29]  Leslie G. Ungerleider,et al.  Neural correlates of category-specific knowledge , 1996, Nature.

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

[31]  N. Logothetis,et al.  Neurophysiology of the BOLD fMRI Signal in Awake Monkeys , 2008, Current Biology.

[32]  G. Schalk,et al.  ELECTROCORTICOGRAPHIC FREQUENCY ALTERATION MAPPING: A CLINICAL TECHNIQUE FOR MAPPING THE MOTOR CORTEX , 2007, Neurosurgery.

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

[34]  J. Fiez Phonology, Semantics, and the Role of the Left Inferior Prefrontal Cortex , 2022 .

[35]  Michael A. DiSano,et al.  Variability of the Relationship between Electrophysiology and BOLD-fMRI across Cortical Regions in Humans , 2011, The Journal of Neuroscience.

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

[37]  David Badre,et al.  Left ventrolateral prefrontal cortex and the cognitive control of memory , 2007, Neuropsychologia.

[38]  Kensuke Kawai,et al.  The dynamics of language-related high-gamma activity assessed on a spatially-normalized brain , 2013, Clinical Neurophysiology.

[39]  Kensuke Kawai,et al.  A Detailed Analysis of Functional Magnetic Resonance Imaging in the Frontal Language Area: A Comparative Study With Extraoperative Electrocortical Stimulation , 2011, Neurosurgery.