Bayesian Modelling of Induced Responses and Neuronal Rhythms

Neural rhythms or oscillations are ubiquitous in neuroimaging data. These spectral responses have been linked to several cognitive processes; including working memory, attention, perceptual binding and neuronal coordination. In this paper, we show how Bayesian methods can be used to finesse the ill-posed problem of reconstructing—and explaining—oscillatory responses. We offer an overview of recent developments in this field, focusing on (i) the use of MEG data and Empirical Bayes to build hierarchical models for group analyses—and the identification of important sources of inter-subject variability and (ii) the construction of novel dynamic causal models of intralaminar recordings to explain layer-specific activity. We hope to show that electrophysiological measurements contain much more spatial information than is often thought: on the one hand, the dynamic causal modelling of non-invasive (low spatial resolution) electrophysiology can afford sub-millimetre (hyper-acute) resolution that is limited only by the (spatial) complexity of the underlying (dynamic causal) forward model. On the other hand, invasive microelectrode recordings (that penetrate different cortical layers) can reveal laminar-specific responses and elucidate hierarchical message passing and information processing within and between cortical regions at a macroscopic scale. In short, the careful and biophysically grounded modelling of sparse data enables one to characterise the neuronal architectures generating oscillations in a remarkable detail.

[1]  Klas H. Pettersen,et al.  Laminar population analysis: estimating firing rates and evoked synaptic activity from multielectrode recordings in rat barrel cortex. , 2007, Journal of neurophysiology.

[2]  Karl J. Friston,et al.  Canonical Microcircuits for Predictive Coding , 2012, Neuron.

[3]  J. Maunsell,et al.  Differences in Gamma Frequencies across Visual Cortex Restrict Their Possible Use in Computation , 2010, Neuron.

[4]  D. Lewis,et al.  GABA neurons and the mechanisms of network oscillations: implications for understanding cortical dysfunction in schizophrenia. , 2008, Schizophrenia bulletin.

[5]  Karl J. Friston,et al.  A dynamic causal model study of neuronal population dynamics , 2010, NeuroImage.

[6]  T. Sejnowski,et al.  Model of Thalamocortical Slow-Wave Sleep Oscillations and Transitions to Activated States , 2002, The Journal of Neuroscience.

[7]  Michelle M. McCarthy,et al.  Therapeutic mechanisms of high-frequency stimulation in Parkinson’s disease and neural restoration via loop-based reinforcement , 2015, Proceedings of the National Academy of Sciences.

[8]  Karl J. Friston,et al.  Multiple sparse priors for the M/EEG inverse problem , 2008, NeuroImage.

[9]  H. Kennedy,et al.  Visual Areas Exert Feedforward and Feedback Influences through Distinct Frequency Channels , 2014, Neuron.

[10]  Karl J. Friston,et al.  Predictive coding under the free-energy principle , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[11]  Simon Kornblith,et al.  Stimulus Load and Oscillatory Activity in Higher Cortex. , 2015, Cerebral cortex.

[12]  Karl J. Friston,et al.  Post hoc Bayesian model selection , 2011, NeuroImage.

[13]  K. D. Singh,et al.  BOLD Responses in Human Primary Visual Cortex are Insensitive to Substantial Changes in Neural Activity , 2013, Front. Hum. Neurosci..

[14]  Kazuhiro Sakamoto,et al.  Spatiotemporal patterns of current source density in the prefrontal cortex of a behaving monkey , 2015, Neural Networks.

[15]  R. Traub,et al.  Inhibition-based rhythms: experimental and mathematical observations on network dynamics. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[16]  Sharp wave-ripple complexes in a reduced model of the hippocampal CA3-CA1 network of the macaque monkey , 2015, BMC Neuroscience.

[17]  J. Pernier,et al.  Stimulus Specificity of Phase-Locked and Non-Phase-Locked 40 Hz Visual Responses in Human , 1996, The Journal of Neuroscience.

[18]  Bijan Pesaran,et al.  Temporal structure in neuronal activity during working memory in macaque parietal cortex , 2000, Nature Neuroscience.

[19]  A. Engel,et al.  Attention to Painful Stimulation Enhances γ-Band Activity and Synchronization in Human Sensorimotor Cortex , 2007, The Journal of Neuroscience.

[20]  Karl J. Friston,et al.  On conductance-based neural field models , 2013, Front. Comput. Neurosci..

[21]  Karl J. Friston,et al.  Dynamic causal modelling of lateral interactions in the visual cortex , 2013, NeuroImage.

[22]  R. Traub,et al.  A model of a CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances. , 1991, Journal of neurophysiology.

[23]  Karl J. Friston,et al.  Variational free energy and the Laplace approximation , 2007, NeuroImage.

[24]  T. Sejnowski,et al.  Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. , 1991, Journal of neurophysiology.

[25]  Dominique L. Pritchett,et al.  Neural Correlates of Tactile Detection: A Combined Magnetoencephalography and Biophysically Based Computational Modeling Study , 2007, The Journal of Neuroscience.

[26]  R. Shapley,et al.  Spatial Spread of the Local Field Potential and its Laminar Variation in Visual Cortex , 2009, The Journal of Neuroscience.

[27]  Gaute T. Einevoll,et al.  Modelling and Analysis of Electrical Potentials Recorded in Microelectrode Arrays (MEAs) , 2015, Neuroinformatics.

[28]  P. Fries,et al.  Robust Gamma Coherence between Macaque V1 and V2 by Dynamic Frequency Matching , 2013, Neuron.

[29]  Eve Marder,et al.  Alternative to hand-tuning conductance-based models: construction and analysis of databases of model neurons. , 2003, Journal of neurophysiology.

[30]  Jim M. Monti,et al.  Neural repetition suppression reflects fulfilled perceptual expectations , 2008, Nature Neuroscience.

[31]  T. Sejnowski,et al.  [Letters to nature] , 1996, Nature.

[32]  Antoine Lutti,et al.  Discrimination of cortical laminae using MEG , 2014, NeuroImage.

[33]  Karl J. Friston,et al.  LFP and oscillations—what do they tell us? , 2015, Current Opinion in Neurobiology.

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

[35]  W. Singer,et al.  Neuronal Dynamics and Neuropsychiatric Disorders: Toward a Translational Paradigm for Dysfunctional Large-Scale Networks , 2012, Neuron.

[36]  T. Sejnowski,et al.  Reduced compartmental models of neocortical pyramidal cells , 1993, Journal of Neuroscience Methods.

[37]  J. Thome,et al.  Current source density analysis of resting state EEG in depression: a review , 2017, Journal of Neural Transmission.

[38]  C. Nicholson,et al.  Experimental optimization of current source-density technique for anuran cerebellum. , 1975, Journal of neurophysiology.

[39]  Adeel Razi,et al.  Bayesian model reduction and empirical Bayes for group (DCM) studies , 2016, NeuroImage.

[40]  J. Schoffelen,et al.  Neuronal Coherence as a Mechanism of Effective Corticospinal Interaction , 2005, Science.

[41]  A. Borst Seeing smells: imaging olfactory learning in bees , 1999, Nature Neuroscience.

[42]  Bernd Lütkenhöner,et al.  Magnetoencephalography and its Achilles' heel , 2003, Journal of Physiology-Paris.

[43]  Karl J. Friston,et al.  Neural masses and fields in dynamic causal modeling , 2013, Front. Comput. Neurosci..

[44]  Abigail Dickinson,et al.  Increased peak gamma frequency in individuals with higher levels of autistic traits , 2015, The European journal of neuroscience.

[45]  P. Fries Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[46]  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.

[47]  Gaute T. Einevoll,et al.  Intrinsic dendritic filtering gives low-pass power spectra of local field potentials , 2010, Journal of Computational Neuroscience.

[48]  R. Desimone,et al.  Gamma-band synchronization in visual cortex predicts speed of change detection , 2006, Nature.

[49]  Karl J. Friston,et al.  Contrast gain control and horizontal interactions in V1: A DCM study , 2014, NeuroImage.

[50]  N. Kopell,et al.  Mixed-mode oscillations in a three time-scale model for the dopaminergic neuron. , 2008, Chaos.

[51]  Khalid Hamandi,et al.  The properties of induced gamma oscillations in human visual cortex show individual variability in their dependence on stimulus size , 2013, NeuroImage.

[52]  W Singer,et al.  Laminar segregation of afferents to lateral geniculate nucleus of the cat: an analysis of current source density. , 1977, Journal of neurophysiology.

[53]  U. Mitzdorf,et al.  Prominent excitatory pathways in the cat visual cortex (A 17 and A 18): A current source density analysis of electrically evoked potentials , 1978, Experimental Brain Research.

[54]  Markus Siegel,et al.  Phase-dependent neuronal coding of objects in short-term memory , 2009, Proceedings of the National Academy of Sciences.

[55]  M. Häusser,et al.  Compartmental models of rat cerebellar Purkinje cells based on simultaneous somatic and dendritic patch‐clamp recordings , 2001, The Journal of physiology.

[56]  Gaute T. Einevoll,et al.  LFPy: a tool for biophysical simulation of extracellular potentials generated by detailed model neurons , 2014, Front. Neuroinform..

[57]  Henry Kennedy,et al.  Cortical High-Density Counterstream Architectures , 2013, Science.

[58]  Karl J. Friston,et al.  The Dynamic Brain: From Spiking Neurons to Neural Masses and Cortical Fields , 2008, PLoS Comput. Biol..

[59]  G. Woodman,et al.  Microcircuitry of Agranular Frontal Cortex: Testing the Generality of the Canonical Cortical Microcircuit , 2014, The Journal of Neuroscience.

[60]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[61]  G. Buzsáki,et al.  Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks , 1995, Current Opinion in Neurobiology.

[62]  Karl J. Friston,et al.  Gamma Oscillations and Neural Field DCMs Can Reveal Cortical Excitability and Microstructure , 2014 .

[63]  Dimitris A Pinotsis,et al.  Extracting novel information from neuroimaging data using neural fields , 2014, BMC Neuroscience.