Response nonlinearities in networks of spiking neurons

Combining information from multiple sources is a fundamental operation performed by networks of neurons in the brain, whose general principles are still largely unknown. Experimental evidence suggests that combination of inputs in cortex relies on nonlinear summation. Such nonlinearities are thought to be fundamental to perform complex computations. However, these non-linearities contradict the balanced-state model, one of the most popular models of cortical dynamics, which predicts networks have a linear response. This linearity is obtained in the limit of very large recurrent coupling strength. We investigate the stationary response of networks of spiking neurons as a function of coupling strength. We show that, while a linear transfer function emerges at strong coupling, nonlinearities are prominent at finite coupling, both at response onset and close to saturation. We derive a general framework to classify nonlinear responses in these networks and discuss which of them can be captured by rate models. This framework could help to understand the observed diversity of non-linearities observed in cortical networks. AUTHOR SUMMARY Models of cortical networks are often studied in the strong coupling limit, where the so-called balanced state emerges. In this strong coupling limit, networks exhibit without fine tuning, a number of ubiquitous properties of cortex, such as the irregular nature of neuronal firing. However, it fails to account for nonlinear summation of inputs, since the strong coupling limit leads to a linear network transfer function. We show that, in networks of spiking neurons, nonlinearities at response-onset and saturation emerge at finite coupling. Critically, for realistic parameter values, both types of nonlinearities are observed at experimentally observed rates. Thus, we propose that these models could explain experimentally observed nonlinearities.

[1]  M. A. Smith,et al.  The spatial structure of correlated neuronal variability , 2016, Nature Neuroscience.

[2]  Nicolas Brunel,et al.  Irregular Persistent Activity Induced by Synaptic Excitatory Feedback , 2007, Frontiers Comput. Neurosci..

[3]  Haim Sompolinsky,et al.  Chaotic Balanced State in a Model of Cortical Circuits , 1998, Neural Computation.

[4]  D. Hansel,et al.  On the Distribution of Firing Rates in Networks of Cortical Neurons , 2011, The Journal of Neuroscience.

[5]  U. Polat,et al.  Collinear stimuli regulate visual responses depending on cell's contrast threshold , 1998, Nature.

[6]  Daniel B. Rubin,et al.  The Stabilized Supralinear Network: A Unifying Circuit Motif Underlying Multi-Input Integration in Sensory Cortex , 2015, Neuron.

[7]  N. Brunel,et al.  Irregular persistent activity induced by synaptic excitatory feedback , 2007, BMC Neuroscience.

[8]  K. H. Britten,et al.  Contrast dependence of response normalization in area MT of the rhesus macaque. , 2002, Journal of neurophysiology.

[9]  J. Poulet,et al.  Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice , 2008, Nature.

[10]  Xiao-Jing Wang,et al.  Mean-Driven and Fluctuation-Driven Persistent Activity in Recurrent Networks , 2007, Neural Computation.

[11]  G. DeAngelis,et al.  A Normalization Model of Multisensory Integration , 2011, Nature Neuroscience.

[12]  Sander W. Keemink,et al.  Behavioral-state modulation of inhibition is context-dependent and cell type specific in mouse visual cortex , 2016, eLife.

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

[14]  David J. Field,et al.  How Close Are We to Understanding V1? , 2005, Neural Computation.

[15]  Cody Baker,et al.  Correlated states in balanced neuronal networks. , 2019, Physical review. E.

[16]  C. Blakemore,et al.  Characteristics of surround inhibition in cat area 17 , 1997, Experimental Brain Research.

[17]  Stephen V. David,et al.  Cortical Membrane Potential Signature of Optimal States for Sensory Signal Detection , 2015, Neuron.

[18]  Carl van Vreeswijk,et al.  Strength of Correlations in Strongly Recurrent Neuronal Networks , 2018, Physical Review X.

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

[20]  Georg B. Keller,et al.  Sensorimotor Mismatch Signals in Primary Visual Cortex of the Behaving Mouse , 2012, Neuron.

[21]  Kenneth D. Miller,et al.  Analysis of the Stabilized Supralinear Network , 2012, Neural Computation.

[22]  T. Hromádka,et al.  Sparse Representation of Sounds in the Unanesthetized Auditory Cortex , 2008, PLoS biology.

[23]  Nicholas J. Priebe,et al.  The Emergence of Contrast-Invariant Orientation Tuning in Simple Cells of Cat Visual Cortex , 2007, Neuron.

[24]  P. Dayan,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S9 References the Asynchronous State in Cortical Circuits , 2022 .

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

[26]  K. Svoboda,et al.  Neural Activity in Barrel Cortex Underlying Vibrissa-Based Object Localization in Mice , 2010, Neuron.

[27]  M. Stryker,et al.  Modulation of Visual Responses by Behavioral State in Mouse Visual Cortex , 2010, Neuron.

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

[29]  Haim Sompolinsky,et al.  Stimulus-dependent suppression of intrinsic variability in recurrent neural networks , 2010, BMC Neuroscience.

[30]  Guillaume Hennequin,et al.  The Dynamical Regime of Sensory Cortex: Stable Dynamics around a Single Stimulus-Tuned Attractor Account for Patterns of Noise Variability , 2018, Neuron.

[31]  Jorge F Mejias,et al.  Paradoxical response reversal of top-down modulation in cortical circuits with three interneuron types. , 2017, eLife.

[32]  K. H. Britten,et al.  Power spectrum analysis of bursting cells in area MT in the behaving monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  Andrew M. Clark,et al.  Stimulus onset quenches neural variability: a widespread cortical phenomenon , 2010, Nature Neuroscience.

[34]  Romain Brette,et al.  Brian 2: an intuitive and efficient neural simulator , 2019, bioRxiv.

[35]  R. Douglas,et al.  A functional microcircuit for cat visual cortex. , 1991, The Journal of physiology.

[36]  Tatjana Tchumatchenko,et al.  Stabilized supralinear network can give rise to bistable, oscillatory, and persistent activity , 2018, Proceedings of the National Academy of Sciences.

[37]  M. Stryker,et al.  A Cortical Circuit for Gain Control by Behavioral State , 2014, Cell.

[38]  J. Hammersley,et al.  Diffusion Processes and Related Topics in Biology , 1977 .

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

[40]  Gianluigi Mongillo,et al.  Bistability and spatiotemporal irregularity in neuronal networks with nonlinear synaptic transmission. , 2012, Physical review letters.

[41]  C. Petersen,et al.  Membrane Potential Dynamics of GABAergic Neurons in the Barrel Cortex of Behaving Mice , 2010, Neuron.

[42]  Rui Luo,et al.  Is My Network Module Preserved and Reproducible? , 2011, PLoS Comput. Biol..

[43]  William R. Softky,et al.  The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  Nicolas Brunel,et al.  Single neuron dynamics and computation , 2014, Current Opinion in Neurobiology.

[45]  Yu Liu,et al.  Motor preparation attenuates neural variability and beta-band LFP in parietal cortex , 2014, Scientific Reports.

[46]  Nicolas Brunel,et al.  Stimulus Dependence of Local Field Potential Spectra: Experiment versus Theory , 2014, The Journal of Neuroscience.

[47]  Romain Brette,et al.  Brian 2, an intuitive and efficient neural simulator , 2019, eLife.

[48]  How gamma-band oscillatory activity participates in encoding of naturalistic stimuli in random networks of excitatory and inhibitory neurons , 2008, BMC Neuroscience.

[49]  Alexander S. Ecker,et al.  Decorrelated Neuronal Firing in Cortical Microcircuits , 2010, Science.

[50]  Carl van Vreeswijk,et al.  Power-Law Input-Output Transfer Functions Explain the Contrast-Response and Tuning Properties of Neurons in Visual Cortex , 2011, PLoS Comput. Biol..

[51]  M. Carandini,et al.  Vision and Locomotion Shape the Interactions between Neuron Types in Mouse Visual Cortex , 2016, Neuron.