How delays matter in an oscillatory whole-brain spiking-neuron network model for MEG alpha-rhythms at rest

In recent years the study of the intrinsic brain dynamics in a relaxed awake state in the absence of any specific task has gained increasing attention, as spontaneous neural activity has been found to be highly structured at a large scale. This so called resting-state activity has been found to be comprised by nonrandom spatiotemporal patterns and fluctuations, and several Resting-State Networks (RSN) have been found in BOLD-fMRI as well as in MEG signal power envelope correlations. The underlying anatomical connectivity structure between areas of the brain has been identified as being a key to the observed functional network connectivity, but the mechanisms behind this are still underdetermined. Theoretical large-scale brain models for fMRI data have corroborated the importance of the connectome in shaping network dynamics, while the importance of delays and noise differ between studies and depend on the models' specific dynamics. In the current study, we present a spiking neuron network model that is able to produce noisy, distributed alpha-oscillations, matching the power peak in the spectrum of group resting-state MEG recordings. We studied how well the model captured the inter-node correlation structure of the alpha-band power envelopes for different delays between brain areas, and found that the model performs best for propagation delays inside the physiological range (5-10 m/s). Delays also shift the transition from noisy to bursting oscillations to higher global coupling values in the model. Thus, in contrast to the asynchronous fMRI state, delays are important to consider in the presence of oscillation.

[1]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[2]  P. Matthews,et al.  Blood oxygenation level dependent contrast resting state networks are relevant to functional activity in the neocortical sensorimotor system , 2005, Experimental Brain Research.

[3]  P. Fransson Spontaneous low‐frequency BOLD signal fluctuations: An fMRI investigation of the resting‐state default mode of brain function hypothesis , 2005, Human brain mapping.

[4]  Matthew J. Brookes,et al.  Measuring functional connectivity using MEG: Methodology and comparison with fcMRI , 2011, NeuroImage.

[5]  A. R. McIntosh,et al.  The effects of physiologically plausible connectivity structure on local and global dynamics in large scale brain models , 2009, Journal of Neuroscience Methods.

[6]  B. Biswal,et al.  Simultaneous assessment of flow and BOLD signals in resting‐state functional connectivity maps , 1997, NMR in biomedicine.

[7]  J. Magee Dendritic integration of excitatory synaptic input , 2000, Nature Reviews Neuroscience.

[8]  Olaf Sporns,et al.  Can structure predict function in the human brain? , 2010, NeuroImage.

[9]  R. Meech,et al.  Calcium-dependent potassium activation in nervous tissues. , 1978, Annual review of biophysics and bioengineering.

[10]  Boris S. Gutkin,et al.  The effects of cholinergic neuromodulation on neuronal phase-response curves of modeled cortical neurons , 2009, Journal of Computational Neuroscience.

[11]  B. Mazoyer,et al.  Cortical networks for working memory and executive functions sustain the conscious resting state in man , 2001, Brain Research Bulletin.

[12]  Mark W. Woolrich,et al.  Inferring task-related networks using independent component analysis in magnetoencephalography , 2012, NeuroImage.

[13]  Cortical network dynamics and response gain , 2010 .

[14]  David B. Roy,et al.  Measuring functional connectivity using long‐term monitoring data , 2011 .

[15]  Viktor K. Jirsa,et al.  Systematic approximations of neural fields through networks of neural masses in the virtual brain , 2013, NeuroImage.

[16]  R. Kötter,et al.  Cortical network dynamics with time delays reveals functional connectivity in the resting brain , 2008, Cognitive Neurodynamics.

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

[18]  William W. Lytton,et al.  Emergence of Physiological Oscillation Frequencies in a Computer Model of Neocortex , 2011, Front. Comput. Neurosci..

[19]  Bruno D. Zumbo,et al.  Bias in Estimation and Hypothesis Testing of Correlation , 2003 .

[20]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[21]  Sacha Jennifer van Albada,et al.  Age trends and sex differences of alpha rhythms including split alpha peaks , 2011, Clinical Neurophysiology.

[22]  F. H. Lopes da Silva,et al.  Model of brain rhythmic activity , 1974, Kybernetik.

[23]  R. Thrall,et al.  Electrophysiological properties of the airway: epithelium in the murine, ovalbumin model of allergic airway disease. , 2004, The American journal of pathology.

[24]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[25]  Gustavo Deco,et al.  Structural connectivity allows for multi-threading during rest: The structure of the cortex leads to efficient alternation between resting state exploratory behavior and default mode processing , 2012, NeuroImage.

[26]  Christof Koch,et al.  Methods in Neuronal Modeling (2nd Edition) , 2000 .

[27]  B. Connors,et al.  Electrophysiological properties of neocortical neurons in vitro. , 1982, Journal of neurophysiology.

[28]  Edward T. Bullmore,et al.  Whole-brain anatomical networks: Does the choice of nodes matter? , 2010, NeuroImage.

[29]  Maurizio Corbetta,et al.  Resting-State Functional Connectivity Emerges from Structurally and Dynamically Shaped Slow Linear Fluctuations , 2013, The Journal of Neuroscience.

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

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

[32]  Liang Wang,et al.  Parcellation‐dependent small‐world brain functional networks: A resting‐state fMRI study , 2009, Human brain mapping.

[33]  B. Sakmann,et al.  Ca2+ buffering and action potential-evoked Ca2+ signaling in dendrites of pyramidal neurons. , 1996, Biophysical journal.

[34]  D. Kleinfeld,et al.  In vivo dendritic calcium dynamics in neocortical pyramidal neurons , 1997, Nature.

[35]  Viktor Jirsa Neural field dynamics with local and global connectivity and time delay , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[36]  Lauren L. Cloutman,et al.  Connectivity-based structural and functional parcellation of the human cortex using diffusion imaging and tractography , 2012, Front. Neuroanat..

[37]  H. Baghdoyan,et al.  Basal forebrain acetylcholine release during REM sleep is significantly greater than during waking. , 2001, American journal of physiology. Regulatory, integrative and comparative physiology.

[38]  Alan C. Evans,et al.  Mapping anatomical connectivity patterns of human cerebral cortex using in vivo diffusion tensor imaging tractography. , 2009, Cerebral cortex.

[39]  J. DeFelipe,et al.  Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters, neuropeptides, calcium-binding proteins, and cell surface molecules. , 1993, Cerebral cortex.

[40]  M. Sarter,et al.  Cortical cholinergic inputs mediating arousal, attentional processing and dreaming: differential afferent regulation of the basal forebrain by telencephalic and brainstem afferents , 1999, Neuroscience.

[41]  V. Haughton,et al.  Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. , 2001, AJNR. American journal of neuroradiology.

[42]  M. Corbetta,et al.  Temporal dynamics of spontaneous MEG activity in brain networks , 2010, Proceedings of the National Academy of Sciences.

[43]  R M Leahy,et al.  A sensor-weighted overlapping-sphere head model and exhaustive head model comparison for MEG. , 1999, Physics in medicine and biology.

[44]  A. Destexhe Kinetic Models of Synaptic Transmission , 1997 .

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

[46]  B. Connors,et al.  Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. , 1991, Science.

[47]  Mingzhou Ding,et al.  Will a large complex system with time delays be stable? , 2004, Physical review letters.

[48]  Xiao-Jing Wang,et al.  Spike-Frequency Adaptation of a Generalized Leaky Integrate-and-Fire Model Neuron , 2004, Journal of Computational Neuroscience.

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

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

[51]  James M. Bower,et al.  Spike Frequency Adaptation Affects the Synchronization Properties of Networks of Cortical Oscillators , 1998, Neural Computation.

[52]  O. Sporns,et al.  Key role of coupling, delay, and noise in resting brain fluctuations , 2009, Proceedings of the National Academy of Sciences.

[53]  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.

[54]  S. Taulu,et al.  Applications of the signal space separation method , 2005, IEEE Transactions on Signal Processing.

[55]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[56]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[57]  M. Steriade Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance. , 1997, Cerebral cortex.

[58]  Gustavo Deco,et al.  Resting brains never rest: computational insights into potential cognitive architectures , 2013, Trends in Neurosciences.

[59]  Viktor K. Jirsa,et al.  Noise during Rest Enables the Exploration of the Brain's Dynamic Repertoire , 2008, PLoS Comput. Biol..

[60]  Xiao-Jing Wang,et al.  Erratum to: Effects of neuromodulation in a cortical network model of object working memory dominated by recurrent inhibition , 2014, Journal of Computational Neuroscience.

[61]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[62]  Srikantan S Nagarajan,et al.  The relationship between magnetic and electrophysiological responses to complex tactile stimuli , 2009, BMC Neuroscience.

[63]  M. P. van den Heuvel,et al.  Normalized Cut Group Clustering of Resting-State fMRI Data , 2008, PloS one.

[64]  V. Haughton,et al.  Mapping functionally related regions of brain with functional connectivity MR imaging. , 2000, AJNR. American journal of neuroradiology.

[65]  G. Edelman,et al.  Large-scale model of mammalian thalamocortical systems , 2008, Proceedings of the National Academy of Sciences.

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

[67]  Klaus Obermayer,et al.  How adaptation shapes spike rate oscillations in recurrent neuronal networks , 2012, Front. Comput. Neurosci..

[68]  Michael Breakspear,et al.  A Canonical Model of Multistability and Scale-Invariance in Biological Systems , 2012, PLoS Comput. Biol..

[69]  J. Shaw,et al.  The brain's alpha rhythms and the mind : a review of classical and modern studies of the alpha rhythm component of the electroencephalogram with commentaries on associated neuroscience and neuropsychology , 2003 .

[70]  R. Llinás The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. , 1988, Science.

[71]  J. C. Anderson,et al.  Estimates of the net excitatory currents evoked by visual stimulation of identified neurons in cat visual cortex. , 1998, Cerebral cortex.

[72]  Edward T. Bullmore,et al.  Efficiency and Cost of Economical Brain Functional Networks , 2007, PLoS Comput. Biol..

[73]  Mark W. Woolrich,et al.  Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? , 2007, NeuroImage.

[74]  M. Lowe,et al.  Functional Connectivity in Single and Multislice Echoplanar Imaging Using Resting-State Fluctuations , 1998, NeuroImage.

[75]  Stephen M. Smith,et al.  fMRI resting state networks define distinct modes of long-distance interactions in the human brain , 2006, NeuroImage.

[76]  C. J. Honeya,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009 .

[77]  Jeff H. Duyn,et al.  Large-scale spontaneous fluctuations and correlations in brain electrical activity observed with magnetoencephalography , 2010, NeuroImage.

[78]  M. Corbetta,et al.  The Dynamical Balance of the Brain at Rest , 2011, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[79]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[80]  Nicolas Brunel,et al.  Encoding of Naturalistic Stimuli by Local Field Potential Spectra in Networks of Excitatory and Inhibitory Neurons , 2008, PLoS Comput. Biol..

[81]  M. Breakspear,et al.  Bistability and Non-Gaussian Fluctuations in Spontaneous Cortical Activity , 2009, The Journal of Neuroscience.

[82]  James A. Roberts,et al.  Biophysical Mechanisms of Multistability in Resting-State Cortical Rhythms , 2011, The Journal of Neuroscience.

[83]  T. Hendler,et al.  Never Resting Brain: Simultaneous Representation of Two Alpha Related Processes in Humans , 2008, PloS one.

[84]  Timothy S. Coalson,et al.  Parcellations and hemispheric asymmetries of human cerebral cortex analyzed on surface-based atlases. , 2012, Cerebral cortex.

[85]  Giulio Tononi,et al.  Modeling sleep and wakefulness in the thalamocortical system. , 2005, Journal of neurophysiology.

[86]  Boris S. Gutkin,et al.  The Effects of Spike Frequency Adaptation and Negative Feedback on the Synchronization of Neural Oscillators , 2001, Neural Computation.

[87]  Henry Markram,et al.  Spike frequency adaptation and neocortical rhythms. , 2002, Journal of neurophysiology.

[88]  G. Deco,et al.  Ongoing Cortical Activity at Rest: Criticality, Multistability, and Ghost Attractors , 2012, The Journal of Neuroscience.

[89]  Mark W. Woolrich,et al.  Measuring functional connectivity in MEG: A multivariate approach insensitive to linear source leakage , 2012, NeuroImage.

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