Modeling mesoscopic cortical dynamics using a mean-field model of conductance-based networks of adaptive exponential integrate-and-fire neurons

Voltage-sensitive dye imaging (VSDi) has revealed fundamental properties of neocortical processing at macroscopic scales. Since for each pixel VSDi signals report the average membrane potential over hundreds of neurons, it seems natural to use a mean-field formalism to model such signals. Here, we present a mean-field model of networks of Adaptive Exponential (AdEx) integrate-and-fire neurons, with conductance-based synaptic interactions. We study a network of regular-spiking (RS) excitatory neurons and fast-spiking (FS) inhibitory neurons. We use a Master Equation formalism, together with a semi-analytic approach to the transfer function of AdEx neurons to describe the average dynamics of the coupled populations. We compare the predictions of this mean-field model to simulated networks of RS-FS cells, first at the level of the spontaneous activity of the network, which is well predicted by the analytical description. Second, we investigate the response of the network to time-varying external input, and show that the mean-field model predicts the response time course of the population. Finally, to model VSDi signals, we consider a one-dimensional ring model made of interconnected RS-FS mean-field units. We found that this model can reproduce the spatio-temporal patterns seen in VSDi of awake monkey visual cortex as a response to local and transient visual stimuli. Conversely, we show that the model allows one to infer physiological parameters from the experimentally-recorded spatio-temporal patterns.

[1]  A. Grinvald,et al.  Imaging Cortical Dynamics at High Spatial and Temporal Resolution with Novel Blue Voltage-Sensitive Dyes , 1999, Neuron.

[2]  Ulrike Goldschmidt,et al.  An Introduction To The Theory Of Point Processes , 2016 .

[3]  Nicolas Brunel,et al.  Fast Global Oscillations in Networks of Integrate-and-Fire Neurons with Low Firing Rates , 1999, Neural Computation.

[4]  A. Grinvald,et al.  Dynamics of Ongoing Activity: Explanation of the Large Variability in Evoked Cortical Responses , 1996, Science.

[5]  Klaus Obermayer,et al.  Low-dimensional spike rate models derived from networks of adaptive integrate-and-fire neurons: Comparison and implementation , 2016, PLoS Comput. Biol..

[6]  C. Petersen,et al.  Visualizing the Cortical Representation of Whisker Touch: Voltage-Sensitive Dye Imaging in Freely Moving Mice , 2006, Neuron.

[7]  Hamutal Slovin,et al.  Population Responses in V1 Encode Different Figures by Response Amplitude , 2015, The Journal of Neuroscience.

[8]  B J Richmond,et al.  Lateral geniculate neurons in behaving primates. III. Response predictions of a channel model with multiple spatial-to-temporal filters. , 1991, Journal of neurophysiology.

[9]  Tim P Vogels,et al.  Signal Propagation and Logic Gating in Networks of Integrate-and-Fire Neurons , 2005, The Journal of Neuroscience.

[10]  Diego Contreras,et al.  Spatiotemporal properties of sensory responses in vivo are strongly dependent on network context , 2012, Front. Syst. Neurosci..

[11]  Pierre Yger,et al.  Topologically invariant macroscopic statistics in balanced networks of conductance-based integrate-and-fire neurons , 2011, Journal of Computational Neuroscience.

[12]  Arvind Kumar,et al.  The High-Conductance State of Cortical Networks , 2008, Neural Computation.

[13]  Hamutal Slovin,et al.  Population response to contextual influences in the primary visual cortex. , 2010, Cerebral cortex.

[14]  Xiao-Jing Wang,et al.  Mean-Field Theory of Irregularly Spiking Neuronal Populations and Working Memory in Recurrent Cortical Networks , 2003 .

[15]  E. Seidemann,et al.  Optimal decoding of correlated neural population responses in the primate visual cortex , 2006, Nature Neuroscience.

[16]  E. Seidemann,et al.  Optimal temporal decoding of neural population responses in a reaction-time visual detection task. , 2008, Journal of neurophysiology.

[17]  F. Chavane,et al.  Imaging cortical correlates of illusion in early visual cortex , 2004, Nature.

[18]  V. Bringuier,et al.  Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. , 1999, Science.

[19]  Wulfram Gerstner,et al.  Adaptive exponential integrate-and-fire model as an effective description of neuronal activity. , 2005, Journal of neurophysiology.

[20]  F. Chavane,et al.  Dynamics of Local Input Normalization Result from Balanced Short- and Long-Range Intracortical Interactions in Area V1 , 2012, The Journal of Neuroscience.

[21]  Esko Valkeila,et al.  An Introduction to the Theory of Point Processes, Volume II: General Theory and Structure, 2nd Edition by Daryl J. Daley, David Vere‐Jones , 2008 .

[22]  F. Chavane,et al.  The stimulus-evoked population response in visual cortex of awake monkey is a propagating wave , 2014, Nature Communications.

[23]  J. Bullier,et al.  Feedforward and feedback connections between areas V1 and V2 of the monkey have similar rapid conduction velocities. , 2001, Journal of neurophysiology.

[24]  Nicolas Brunel,et al.  Dynamics of Networks of Excitatory and Inhibitory Neurons in Response to Time-Dependent Inputs , 2011, Front. Comput. Neurosci..

[25]  Frédéric Chavane,et al.  A biophysical cortical column model to study the multi-component origin of the VSDI signal , 2010, NeuroImage.

[26]  James G. King,et al.  Reconstruction and Simulation of Neocortical Microcircuitry , 2015, Cell.

[27]  M. Bennett,et al.  Relative conduction velocities of small myelinated and non-myelinated fibres in the central nervous system. , 1972, Nature: New biology.

[28]  H. Sompolinsky,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 1996, Science.

[29]  Nicolas Brunel,et al.  Dynamics of Sparsely Connected Networks of Excitatory and Inhibitory Spiking Neurons , 2000, Journal of Computational Neuroscience.

[30]  A. Destexhe,et al.  Heterogeneous firing rate response of mouse layer V pyramidal neurons in the fluctuation‐driven regime , 2016, The Journal of physiology.

[31]  Alex S. Ferecskó,et al.  Model‐based analysis of excitatory lateral connections in the visual cortex , 2006, The Journal of comparative neurology.

[32]  Haim Sompolinsky,et al.  Chaos and synchrony in a model of a hypercolumn in visual cortex , 1996, Journal of Computational Neuroscience.

[33]  D. Amit,et al.  Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex. , 1997, Cerebral cortex.

[34]  A. Destexhe,et al.  The high-conductance state of neocortical neurons in vivo , 2003, Nature Reviews Neuroscience.

[35]  Jean Bennett,et al.  Lateral Connectivity and Contextual Interactions in Macaque Primary Visual Cortex , 2002, Neuron.

[36]  Thomas K. Berger,et al.  Combined voltage and calcium epifluorescence imaging in vitro and in vivo reveals subthreshold and suprathreshold dynamics of mouse barrel cortex. , 2007, Journal of neurophysiology.

[37]  Romain Brette,et al.  The Brian Simulator , 2009, Front. Neurosci..

[38]  Yuzhi Chen,et al.  Sensory stimulation shifts visual cortex from synchronous to asynchronous states , 2014, Nature.

[39]  D. Contreras,et al.  Voltage-Sensitive Dye Imaging of Neocortical Spatiotemporal Dynamics to Afferent Activation Frequency , 2001, The Journal of Neuroscience.

[40]  M. Steriade,et al.  Natural waking and sleep states: a view from inside neocortical neurons. , 2001, Journal of neurophysiology.

[41]  Athanasios Papoulis,et al.  Probability, Random Variables and Stochastic Processes , 1965 .

[42]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

[43]  Alain Destexhe,et al.  A Master Equation Formalism for Macroscopic Modeling of Asynchronous Irregular Activity States , 2009, Neural Computation.

[44]  Romain Brette,et al.  A Threshold Equation for Action Potential Initiation , 2010, PLoS Comput. Biol..

[45]  M. Scanziani,et al.  Distinct recurrent versus afferent dynamics in cortical visual processing , 2015, Nature Neuroscience.

[46]  Amiram Grinvald,et al.  Dural substitute for long-term imaging of cortical activity in behaving monkeys and its clinical implications , 2002, Journal of Neuroscience Methods.

[47]  I. Miller Probability, Random Variables, and Stochastic Processes , 1966 .

[48]  H. Markram,et al.  Interneurons of the neocortical inhibitory system , 2004, Nature Reviews Neuroscience.

[49]  Frédéric Chavane,et al.  Effects of GABAA kinetics on cortical population activity: computational studies and physiological confirmations. , 2016, Journal of neurophysiology.

[50]  Xiao-Jing Wang,et al.  What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. , 2003, Journal of neurophysiology.

[51]  A. Aertsen,et al.  Neuronal Integration of Synaptic Input in the Fluctuation-Driven Regime , 2004, The Journal of Neuroscience.

[52]  B. Richmond,et al.  Intrinsic dynamics in neuronal networks. I. Theory. , 2000, Journal of neurophysiology.

[53]  J. B. Levitt,et al.  Circuits for Local and Global Signal Integration in Primary Visual Cortex , 2002, The Journal of Neuroscience.