Frequency-specific electrophysiologic correlates of resting state fMRI networks

ABSTRACT Resting state functional MRI (R‐fMRI) studies have shown that slow (<0.1 Hz), intrinsic fluctuations of the blood oxygen level dependent (BOLD) signal are temporally correlated within hierarchically organized functional systems known as resting state networks (RSNs) (Doucet et al., 2011). Most broadly, this hierarchy exhibits a dichotomy between two opposed systems (Fox et al., 2005). One system engages with the environment and includes the visual, auditory, and sensorimotor (SMN) networks as well as the dorsal attention network (DAN), which controls spatial attention. The other system includes the default mode network (DMN) and the fronto‐parietal control system (FPC), RSNs that instantiate episodic memory and executive control, respectively. Here, we test the hypothesis, based on the spectral specificity of electrophysiologic responses to perceptual vs. memory tasks (Klimesch, 1999; Pfurtscheller and Lopes da Silva, 1999), that these two large‐scale neural systems also manifest frequency specificity in the resting state. We measured the spatial correspondence between electrocorticographic (ECoG) band‐limited power (BLP) and R‐fMRI correlation patterns in awake, resting, human subjects. Our results show that, while gamma BLP correspondence was common throughout the brain, theta (4–8 Hz) BLP correspondence was stronger in the DMN and FPC, whereas alpha (8–12 Hz) correspondence was stronger in the SMN and DAN. Thus, the human brain, at rest, exhibits frequency specific electrophysiology, respecting both the spectral structure of task responses and the hierarchical organization of RSNs. HighlightsThe first systematic analysis of spectral specificity in ECoG:R‐fMRI correspondence.ECoG:fMRI correspondence was found in gamma frequencies in all RSNs.Theta (4–8 Hz) BLP:fMRI correspondence was stronger in the DMN and FPC.Alpha (8–12 Hz) BLP:fMRI correspondence was stronger in the SMN and DAN.Spectral specificity of intrinsic electrophysiology matches RSN hierarchy.

[1]  S. Raghavachari,et al.  Gating of Human Theta Oscillations by a Working Memory Task , 2001, The Journal of Neuroscience.

[2]  Jonathan Winawer,et al.  Asynchronous Broadband Signals Are the Principal Source of the BOLD Response in Human Visual Cortex , 2013, Current Biology.

[3]  Saskia Haegens,et al.  Inter- and intra-individual variability in alpha peak frequency , 2014, NeuroImage.

[4]  Bart Gips,et al.  Temporal coding organized by coupled alpha and gamma oscillations prioritize visual processing , 2014, Trends in Neurosciences.

[5]  N. E. Crone,et al.  PW5-2 Shifts in gamma phase-amplitude coupling frequency from theta to alpha over posterior cortex during visual tasks , 2010, Clinical Neurophysiology.

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

[7]  Shangkai Gao,et al.  Fast presurgical functional mapping using task-related intracranial high gamma activity. , 2013, Journal of neurosurgery.

[8]  Marc W Howard,et al.  Theta and Gamma Oscillations during Encoding Predict Subsequent Recall , 2003, The Journal of Neuroscience.

[9]  I. Fried,et al.  Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex , 2008, Nature Neuroscience.

[10]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[11]  Josef Parvizi,et al.  Resting oscillations and cross-frequency coupling in the human posteromedial cortex , 2012, NeuroImage.

[12]  Marcus E Raichle,et al.  A Paradigm Shift in Functional Brain Imaging , 2009, The Journal of Neuroscience.

[13]  Zhishun Wang,et al.  Visual inspection of independent components: Defining a procedure for artifact removal from fMRI data , 2010, Journal of Neuroscience Methods.

[14]  Charan Ranganath,et al.  Frontal midline theta oscillations during working memory maintenance and episodic encoding and retrieval , 2014, NeuroImage.

[15]  John J. Foxe,et al.  Propagating Neocortical Gamma Bursts Are Coordinated by Traveling Alpha Waves , 2013, The Journal of Neuroscience.

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

[17]  I. Fried,et al.  A Widely Distributed Spectral Signature of Task-Negative Electrocorticography Responses Revealed during a Visuomotor Task in the Human Cortex , 2012, The Journal of Neuroscience.

[18]  R. Knight,et al.  Shifts in Gamma Phase–Amplitude Coupling Frequency from Theta to Alpha Over Posterior Cortex During Visual Tasks , 2010, Front. Hum. Neurosci..

[19]  M. Mishkin,et al.  Spontaneous High-Gamma Band Activity Reflects Functional Organization of Auditory Cortex in the Awake Macaque , 2012, Neuron.

[20]  Simon Hanslmayr,et al.  Neural Communication Patterns Underlying Conflict Detection, Resolution, and Adaptation , 2014, The Journal of Neuroscience.

[21]  M. Frank,et al.  Frontal theta as a mechanism for cognitive control , 2014, Trends in Cognitive Sciences.

[22]  Justin L. Vincent,et al.  Distinct cortical anatomy linked to subregions of the medial temporal lobe revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

[23]  M. Raichle,et al.  Anatomic Localization and Quantitative Analysis of Gradient Refocused Echo-Planar fMRI Susceptibility Artifacts , 1997, NeuroImage.

[24]  Carl D. Hacker,et al.  Clustering of Resting State Networks , 2012, PloS one.

[25]  L. Colgin.  Mechanisms and functions of theta rhythms. , 2013, Annual review of neuroscience.

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

[27]  Kareem A. Zaghloul,et al.  Decreases in theta and increases in high frequency activity underlie associative memory encoding , 2015, NeuroImage.

[28]  K. Meador,et al.  Theta oscillations mediate interaction between prefrontal cortex and medial temporal lobe in human memory. , 2010, Cerebral cortex.

[29]  R. Knight,et al.  The functional role of cross-frequency coupling , 2010, Trends in Cognitive Sciences.

[30]  HighWire Press.  The journal of neuroscience : the official journal of the Society for Neuroscience. , 1981 .

[31]  N. Logothetis,et al.  Very slow activity fluctuations in monkey visual cortex: implications for functional brain imaging. , 2003, Cerebral cortex.

[32]  Dietmar Cordes,et al.  Hierarchical clustering to measure connectivity in fMRI resting-state data. , 2002, Magnetic resonance imaging.

[33]  L. Lemieux,et al.  With or without spikes: localization of focal epileptic activity by simultaneous electroencephalography and functional magnetic resonance imaging. , 2011, Brain : a journal of neurology.

[34]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[35]  A. Engel,et al.  Intrinsic Coupling Modes: Multiscale Interactions in Ongoing Brain Activity , 2013, Neuron.

[36]  Gabriele Arnulfo,et al.  Phase and amplitude correlations in resting-state activity in human stereotactical EEG recordings , 2015, NeuroImage.

[37]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[38]  R. Leahy,et al.  Multiple Dipole Modeling and Localization from , 1992 .

[39]  Adrian L. Williams,et al.  Task-Related Changes in Cortical Synchronization Are Spatially Coincident with the Hemodynamic Response , 2002, NeuroImage.

[40]  W. Klimesch.  EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[41]  Simon Hanslmayr,et al.  Human Hippocampal Dynamics during Response Conflict , 2015, Current Biology.

[42]  Rajesh P. N. Rao,et al.  Broadband changes in the cortical surface potential track activation of functionally diverse neuronal populations , 2014, NeuroImage.

[43]  B. T. Thomas Yeo,et al.  Borders, map clusters, and supra-areal organization in visual cortex , 2014, NeuroImage.

[44]  Mark Jenkinson,et al.  The minimal preprocessing pipelines for the Human Connectome Project , 2013, NeuroImage.

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

[46]  D. Leopold,et al.  Layer-Specific Entrainment of Gamma-Band Neural Activity by the Alpha Rhythm in Monkey Visual Cortex , 2012, Current Biology.

[47]  Timothy O. Laumann,et al.  Methods to detect, characterize, and remove motion artifact in resting state fMRI , 2014, NeuroImage.

[48]  Hellmuth Obrig,et al.  Stimulus-Induced and State-Dependent Sustained Gamma Activity Is Tightly Coupled to the Hemodynamic Response in Humans , 2009, The Journal of Neuroscience.

[49]  G. Buzsáki,et al.  Mechanisms of gamma oscillations. , 2012, Annual review of neuroscience.

[50]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: I. Increases in Subcortical Structures and Cerebellum but Not in Nonvisual Cortex , 1997, Journal of Cognitive Neuroscience.

[51]  Stefan Rampp,et al.  Slow-theta power decreases during item-place encoding predict spatial accuracy of subsequent context recall , 2016, NeuroImage.

[52]  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.

[53]  Nasser Kehtarnavaz,et al.  Average field map image template for Echo-Planar image analysis , 2008, 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[54]  K. Miller,et al.  Human Retrosplenial Cortex Displays Transient Theta Phase Locking with Medial Temporal Cortex Prior to Activation during Autobiographical Memory Retrieval , 2013, The Journal of Neuroscience.

[55]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[56]  Rajesh P. N. Rao,et al.  Spectral Changes in Cortical Surface Potentials during Motor Movement , 2007, The Journal of Neuroscience.

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

[58]  M. Corbetta,et al.  A Cortical Core for Dynamic Integration of Functional Networks in the Resting Human Brain , 2012, Neuron.

[59]  A. Karim,et al.  Brain Oscillatory Substrates of Visual Short-Term Memory Capacity , 2009, Current Biology.

[60]  Robert T. Knight,et al.  Spatial and temporal relationships of electrocorticographic alpha and gamma activity during auditory processing , 2014, NeuroImage.

[61]  Biyu J. He,et al.  Electrophysiological correlates of the brain's intrinsic large-scale functional architecture , 2008, Proceedings of the National Academy of Sciences.

[62]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[63]  Carl D. Hacker,et al.  Resting state network estimation in individual subjects , 2013, NeuroImage.

[64]  Arne D. Ekstrom,et al.  Multifaceted roles for low-frequency oscillations in bottom-up and top-down processing during navigation and memory , 2014, NeuroImage.

[65]  Sabine Kastner,et al.  Electrophysiological Low-Frequency Coherence and Cross-Frequency Coupling Contribute to BOLD Connectivity , 2012, Neuron.

[66]  Joseph R. Madsen,et al.  Human theta oscillations exhibit task dependence during virtual maze navigation , 1999, Nature.

[67]  N. Logothetis,et al.  Scaling Brain Size, Keeping Timing: Evolutionary Preservation of Brain Rhythms , 2013, Neuron.

[68]  G. Buzsáki,et al.  Memory, navigation and theta rhythm in the hippocampal-entorhinal system , 2013, Nature Neuroscience.

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

[70]  Matthew J. Brookes,et al.  The relationship between MEG and fMRI , 2014, NeuroImage.

[71]  Kurt E. Weaver,et al.  Identifying Functional Networks Using Endogenous Connectivity in Gamma Band Electrocorticography , 2013, Brain Connect..

[72]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[73]  R. Adolphs,et al.  The social brain: neural basis of social knowledge. , 2009, Annual review of psychology.

[74]  M. Corbetta,et al.  Large-scale cortical correlation structure of spontaneous oscillatory activity , 2012, Nature Neuroscience.

[75]  Michael J Kahana,et al.  Human intracranial high-frequency activity during memory processing: neural oscillations or stochastic volatility? , 2015, Current Opinion in Neurobiology.

[76]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

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

[78]  M. Kahana,et al.  Phase–Amplitude Coupling in Human Electrocorticography Is Spatially Distributed and Phase Diverse , 2012, The Journal of Neuroscience.

[79]  A. Snyder,et al.  Longitudinal analysis of neural network development in preterm infants. , 2010, Cerebral cortex.

[80]  G. Buzsáki.  Theta Oscillations in the Hippocampus , 2002, Neuron.

[81]  Arne D. Ekstrom,et al.  A comparative study of human and rat hippocampal low‐frequency oscillations during spatial navigation , 2013, Hippocampus.

[82]  Olaf Hauk,et al.  Comparison of noise-normalized minimum norm estimates for MEG analysis using multiple resolution metrics , 2011, NeuroImage.

[83]  Marc Joliot,et al.  Brain activity at rest: a multiscale hierarchical functional organization. , 2011, Journal of neurophysiology.

[84]  Abraham Z. Snyder,et al.  Frequency specific interactions of MEG resting state activity within and across brain networks as revealed by the multivariate interaction measure , 2013, NeuroImage.

[85]  R. Oostenveld,et al.  I see what you mean: Theta power increases are involved in the retrieval of lexical semantic information , 2008, Brain and Language.

[86]  P. Uhlhaas,et al.  Working memory and neural oscillations: alpha–gamma versus theta–gamma codes for distinct WM information? , 2014, Trends in Cognitive Sciences.

[87]  Efstathios D. Gennatas,et al.  Network-level structural covariance in the developing brain , 2010, Proceedings of the National Academy of Sciences.

[88]  B. Foster,et al.  Intrinsic and Task-Dependent Coupling of Neuronal Population Activity in Human Parietal Cortex , 2015, Neuron.

[89]  David M. Groppe,et al.  Neurophysiological Investigation of Spontaneous Correlated and Anticorrelated Fluctuations of the BOLD Signal , 2013, The Journal of Neuroscience.

[90]  M. Kahana,et al.  Slow-Theta-to-Gamma Phase-Amplitude Coupling in Human Hippocampus Supports the Formation of New Episodic Memories. , 2016, Cerebral cortex.

[91]  Pascal Fries,et al.  Stimulus-induced visual cortical networks are recapitulated by spontaneous local and interareal synchronization , 2015, Proceedings of the National Academy of Sciences.

[92]  R. Knight,et al.  Oscillatory Dynamics of Prefrontal Cognitive Control , 2016, Trends in Cognitive Sciences.

[93]  Joerg F. Hipp,et al.  BOLD fMRI Correlation Reflects Frequency-Specific Neuronal Correlation , 2015, Current Biology.

[94]  Darren Price,et al.  Investigating the electrophysiological basis of resting state networks using magnetoencephalography , 2011, Proceedings of the National Academy of Sciences.

[95]  P. M. Gleiser,et al.  Modelling hierarchical structure in functional brain networks , 2010, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[96]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[97]  Marcel van Gerven,et al.  Measuring directionality between neuronal oscillations of different frequencies , 2015, NeuroImage.

[98]  David A. Leopold,et al.  The contribution of electrophysiology to functional connectivity mapping , 2013, NeuroImage.

[99]  Arne D. Ekstrom,et al.  Frequency–specific network connectivity increases underlie accurate spatiotemporal memory retrieval , 2013, Nature Neuroscience.

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