Electrophysiological Low-Frequency Coherence and Cross-Frequency Coupling Contribute to BOLD Connectivity

Brain networks are commonly defined using correlations between blood oxygen level-dependent (BOLD) signals in different brain areas. Although evidence suggests that gamma-band (30-100 Hz) neural activity contributes to local BOLD signals, the neural basis of interareal BOLD correlations is unclear. We first defined a visual network in monkeys based on converging evidence from interareal BOLD correlations during a fixation task, task-free state, and anesthesia, and then simultaneously recorded local field potentials (LFPs) from the same four network areas in the task-free state. Low-frequency oscillations (<20 Hz), and not gamma activity, predominantly contributed to interareal BOLD correlations. The low-frequency oscillations also influenced local processing by modulating gamma activity within individual areas. We suggest that such cross-frequency coupling links local BOLD signals to BOLD correlations across distributed networks.

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

[2]  Ankoor S. Shah,et al.  An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. , 2005, Journal of neurophysiology.

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

[4]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

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

[6]  R W Cox,et al.  Real‐time 3D image registration for functional MRI , 1999, Magnetic resonance in medicine.

[7]  D. McCormick,et al.  Sleep and arousal: thalamocortical mechanisms. , 1997, Annual review of neuroscience.

[8]  Michael X Cohen,et al.  Assessing transient cross-frequency coupling in EEG data , 2008, Journal of Neuroscience Methods.

[9]  Vincenzo Crunelli,et al.  Infraslow (<0.1 Hz) oscillations in thalamic relay nuclei basic mechanisms and significance to health and disease states. , 2011, Progress in brain research.

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

[11]  Diane M. Beck,et al.  To See or Not to See: Prestimulus α Phase Predicts Visual Awareness , 2009, The Journal of Neuroscience.

[12]  E. Jones,et al.  Comprar The Thalamus 2 Volume Set | Edward G. Jones | 9780521858816 | Cambridge University Press , 2007 .

[13]  Clara A. Scholl,et al.  Synchronized delta oscillations correlate with the resting-state functional MRI signal , 2007, Proceedings of the National Academy of Sciences.

[14]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

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

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

[17]  Mark W. Woolrich,et al.  Network modelling methods for FMRI , 2011, NeuroImage.

[18]  M. Schölvinck,et al.  Neural basis of global resting-state fMRI activity , 2010, Proceedings of the National Academy of Sciences.

[19]  N. Logothetis,et al.  Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1 , 2006, Nature Neuroscience.

[20]  Mingzhou Ding,et al.  Attentional Modulation of Alpha Oscillations in Macaque Inferotemporal Cortex , 2011, The Journal of Neuroscience.

[21]  N. Logothetis,et al.  A combined MRI and histology atlas of the rhesus monkey brain in stereotaxic coordinates , 2007 .

[22]  Mark W. Woolrich,et al.  Bayesian analysis of neuroimaging data in FSL , 2009, NeuroImage.

[23]  Olaf Sporns,et al.  Network structure of cerebral cortex shapes functional connectivity on multiple time scales , 2007, Proceedings of the National Academy of Sciences.

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

[25]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

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

[27]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[28]  M. Greicius.  Resting-state functional connectivity in neuropsychiatric disorders , 2008, Current opinion in neurology.

[29]  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.

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

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

[32]  P. König,et al.  Top-down processing mediated by interareal synchronization. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[33]  S. Hughes,et al.  Synchronized Oscillations at α and θ Frequencies in the Lateral Geniculate Nucleus , 2004, Neuron.

[34]  S. Hughes,et al.  Thalamic Mechanisms of EEG Alpha Rhythms and Their Pathological Implications , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[35]  J. Palva,et al.  Very Slow EEG Fluctuations Predict the Dynamics of Stimulus Detection and Oscillation Amplitudes in Humans , 2008, The Journal of Neuroscience.

[36]  P. Jezzard,et al.  Correction for geometric distortion in echo planar images from B0 field variations , 1995, Magnetic resonance in medicine.

[37]  Xiao-Jing Wang.  Neurophysiological and computational principles of cortical rhythms in cognition. , 2010, Physiological reviews.

[38]  A. Engel,et al.  Spectral fingerprints of large-scale neuronal interactions , 2012, Nature Reviews Neuroscience.

[39]  R. Desimone,et al.  Laminar differences in gamma and alpha coherence in the ventral stream , 2011, Proceedings of the National Academy of Sciences.

[40]  C. Schroeder,et al.  Neuronal Mechanisms of Cortical Alpha Oscillations in Awake-Behaving Macaques , 2008, The Journal of Neuroscience.

[41]  Jonathan D. Power,et al.  Prediction of Individual Brain Maturity Using fMRI , 2010, Science.

[42]  Y. Saalmann,et al.  The Pulvinar Regulates Information Transmission Between Cortical Areas Based on Attention Demands , 2012, Science.

[43]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[44]  M. Carandini,et al.  Local Origin of Field Potentials in Visual Cortex , 2009, Neuron.

[45]  S Shipp,et al.  The functional logic of cortico-pulvinar connections. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[46]  S. Hughes,et al.  Synchronized oscillations at alpha and theta frequencies in the lateral geniculate nucleus. , 2004, Neuron.

[47]  Kevin J Black,et al.  Atlas template images for nonhuman primate neuroimaging: baboon and macaque. , 2004, Methods in enzymology.

[48]  J. Schoffelen,et al.  Comparing spectra and coherences for groups of unequal size , 2007, Journal of Neuroscience Methods.

[49]  Trichur Raman Vidyasagar,et al.  A minimally invasive and reversible system for chronic recordings from multiple brain sites in macaque monkeys , 2009, Journal of Neuroscience Methods.

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

[51]  P. Matthews,et al.  Neuroimaging: Applications of fMRI in translational medicine and clinical practice , 2006, Nature Reviews Neuroscience.

[52]  W. Singer,et al.  Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex , 1991, Science.

[53]  N. Franks.  General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal , 2008, Nature Reviews Neuroscience.

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

[55]  David A. Leopold,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[56]  I. G. Sil’kis,et al.  Background gamma-oscillations in neuronal networks with interhemisphere connections , 1998, Neuroscience and Behavioral Physiology.

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

[58]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[59]  R. VanRullen,et al.  An oscillatory mechanism for prioritizing salient unattended stimuli , 2012, Trends in Cognitive Sciences.

[60]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[61]  F. H. Lopes da Silva,et al.  Relative contributions of intracortical and thalamo-cortical processes in the generation of alpha rhythms, revealed by partial coherence analysis. , 1980, Electroencephalography and clinical neurophysiology.

[62]  Sabine Kastner,et al.  Methods for functional magnetic resonance imaging in normal and lesioned behaving monkeys , 2005, Journal of Neuroscience Methods.

[63]  Warren M. Grill.  Exploring the Thalamus and Its Role in Cortical Function.Second Edition.ByS Murray Shermanand, R W Guillery.Cambridge (Massachusetts): MIT Press.$65.00. xxiii + 484 p; ill.; index. ISBN: 0‐262‐19532‐1. 2006. , 2007 .

[64]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[65]  Mark Jenkinson,et al.  Improved unwarping of EPI images using regularised B0 maps , 2001, NeuroImage.

[66]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[67]  Vincenzo Crunelli,et al.  Cellular Dynamics of Cholinergically Induced α (8–13 Hz) Rhythms in Sensory Thalamic Nuclei In Vitro , 2008, The Journal of Neuroscience.

[68]  A. von Stein,et al.  Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[69]  R. VanRullen,et al.  The phase of ongoing EEG oscillations predicts visual perception , 2010 .

[70]  Gustavo Deco,et al.  Role of local network oscillations in resting-state functional connectivity , 2011, NeuroImage.

[71]  G. Buzsáki,et al.  A 4 Hz Oscillation Adaptively Synchronizes Prefrontal, VTA, and Hippocampal Activities , 2011, Neuron.

[72]  N. Logothetis,et al.  The Amplitude and Timing of the BOLD Signal Reflects the Relationship between Local Field Potential Power at Different Frequencies , 2012, The Journal of Neuroscience.

[73]  G. Karmos,et al.  Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection , 2008, Science.

[74]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.

[75]  Alpha rhythm in the cat thalamus. , 1993, Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie.

[76]  Liang Wang,et al.  Dynamic functional reorganization of the motor execution network after stroke. , 2010, Brain : a journal of neurology.

[77]  M. Fox,et al.  Intrinsic functional relations between human cerebral cortex and thalamus. , 2008, Journal of neurophysiology.

[78]  Xiaoping P. Hu,et al.  Comparison of alpha-chloralose, medetomidine and isoflurane anesthesia for functional connectivity mapping in the rat. , 2010, Magnetic resonance imaging.

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

[80]  F. D. Silva.  Neural mechanisms underlying brain waves: from neural membranes to networks. , 1991 .

[81]  Sonja Grün,et al.  How local is the local field potential? , 2011, BMC Neuroscience.

[82]  P. Mitra,et al.  Analysis of dynamic brain imaging data. , 1998, Biophysical journal.

[83]  F. L. D. Silva,et al.  The cortical source of the alpha rhythm , 1977, Neuroscience Letters.

[84]  J. Palva,et al.  Functional Roles of Alpha-Band Phase Synchronization in Local and Large-Scale Cortical Networks , 2011, Front. Psychology.

[85]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[86]  A Nishimoto,et al.  Thalamic control of spontaneous alpha-rhythm and evoked responses. , 1978, Applied neurophysiology.

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

[88]  M. Raichle,et al.  Rat brains also have a default mode network , 2012, Proceedings of the National Academy of Sciences.

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

[90]  Robert Desimone,et al.  Cortical Connections of Area V4 in the Macaque , 2008 .

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

[92]  Justin L. Vincent,et al.  Intrinsic functional architecture in the anaesthetized monkey brain , 2007, Nature.

[93]  M. Raichle,et al.  Disease and the brain's dark energy , 2010, Nature Reviews Neurology.

[94]  G. Ermentrout,et al.  Gamma rhythms and beta rhythms have different synchronization properties. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[95]  Doris Y. Tsao,et al.  Functional Connectivity of the Macaque Brain across Stimulus and Arousal States , 2009, The Journal of Neuroscience.

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

[97]  R. Llinás,et al.  The functional states of the thalamus and the associated neuronal interplay. , 1988, Physiological reviews.

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

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

[100]  D. Hubel,et al.  The role of fixational eye movements in visual perception , 2004, Nature Reviews Neuroscience.

[101]  Partha P. Mitra,et al.  Chronux: A platform for analyzing neural signals , 2010, Journal of Neuroscience Methods.

[102]  O. Jensen,et al.  Cross-frequency coupling between neuronal oscillations , 2007, Trends in Cognitive Sciences.

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

[104]  M. Pinsk,et al.  Visuotopic Organization of Macaque Posterior Parietal Cortex: A Functional Magnetic Resonance Imaging Study , 2011, The Journal of Neuroscience.