Role of Input Correlations in Shaping the Variability and Noise Correlations of Evoked Activity in the Neocortex

Recent analysis of evoked activity recorded across different brain regions and tasks revealed a marked decrease in noise correlations and trial-by-trial variability. Given the importance of correlations and variability for information processing within the rate coding paradigm, several mechanisms have been proposed to explain the reduction in these quantities despite an increase in firing rates. These models suggest that anatomical clusters and/or tightly balanced excitation–inhibition can generate intrinsic network dynamics that may exhibit a reduction in noise correlations and trial-by-trial variability when perturbed by an external input. Such mechanisms based on the recurrent feedback crucially ignore the contribution of feedforward input to the statistics of the evoked activity. Therefore, we investigated how statistical properties of the feedforward input shape the statistics of the evoked activity. Specifically, we focused on the effect of input correlation structure on the noise correlations and trial-by-trial variability. We show that the ability of neurons to transfer the input firing rate, correlation, and variability to the output depends on the correlations within the presynaptic pool of a neuron, and that an input with even weak within-correlations can be sufficient to reduce noise correlations and trial-by-trial variability, without requiring any specific recurrent connectivity structure. In general, depending on the ongoing activity state, feedforward input could either increase or decrease noise correlation and trial-by-trial variability. Thus, we propose that evoked activity statistics are jointly determined by the feedforward and feedback inputs.

[1]  Peter Dayan,et al.  The Effect of Correlated Variability on the Accuracy of a Population Code , 1999, Neural Computation.

[2]  Douglas A Ruff,et al.  Attention can increase or decrease spike count correlations between pairs of neurons depending on their role in a task , 2014, Nature Neuroscience.

[3]  Marc-Oliver Gewaltig,et al.  NEST (NEural Simulation Tool) , 2007, Scholarpedia.

[4]  Robert Rosenbaum,et al.  Frontiers in Computational Neuroscience Computational Neuroscience , 2022 .

[5]  Laurent U. Perrinet,et al.  Complex dynamics in recurrent cortical networks based on spatially realistic connectivities , 2012, Front. Comput. Neurosci..

[6]  József Fiser,et al.  Suppression of cortical neural variability is stimulus- and state-dependent. , 2012, Journal of neurophysiology.

[7]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[8]  Stefan Rotter,et al.  Higher-Order Statistics of Input Ensembles and the Response of Simple Model Neurons , 2003, Neural Computation.

[9]  Romain Brette,et al.  Generation of Correlated Spike Trains , 2009, Neural Computation.

[10]  Robert Rosenbaum,et al.  Mechanisms That Modulate the Transfer of Spiking Correlations , 2011, Neural Computation.

[11]  M. A. Smith,et al.  Spatial and Temporal Scales of Neuronal Correlation in Primary Visual Cortex , 2008, The Journal of Neuroscience.

[12]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[13]  Sonja Grün,et al.  Can Spike Coordination Be Differentiated from Rate Covariation? , 2008, Neural Computation.

[14]  Nikos Yannaros On Cox processes and gamma renewal processes , 1988, Journal of Applied Probability.

[15]  Jude F. Mitchell,et al.  Attentional Modulation of Firing Rate Varies with Burstiness across Putative Pyramidal Neurons in Macaque Visual Area V4 , 2011, The Journal of Neuroscience.

[16]  T. Sejnowski,et al.  Impact of Correlated Synaptic Input on Output Firing Rate and Variability in Simple Neuronal Models , 2000, The Journal of Neuroscience.

[17]  Jude F. Mitchell,et al.  Differential Attention-Dependent Response Modulation across Cell Classes in Macaque Visual Area V4 , 2007, Neuron.

[18]  Robert Rosenbaum,et al.  The Effects of Pooling on Spike Train Correlations , 2011, Front. Neurosci..

[19]  K. Harris,et al.  Cortical state and attention , 2011, Nature Reviews Neuroscience.

[20]  Arvind Kumar,et al.  Significance of Input Correlations in Striatal Function , 2011, PLoS Comput. Biol..

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

[22]  A. Aertsen,et al.  Spiking activity propagation in neuronal networks: reconciling different perspectives on neural coding , 2010, Nature Reviews Neuroscience.

[23]  A. Pouget,et al.  Neural correlations, population coding and computation , 2006, Nature Reviews Neuroscience.

[24]  J. Maunsell,et al.  Attention improves performance primarily by reducing interneuronal correlations , 2009, Nature Neuroscience.

[25]  John D. Hunter,et al.  Matplotlib: A 2D Graphics Environment , 2007, Computing in Science & Engineering.

[26]  Terrence J. Sejnowski,et al.  Integrate-and-Fire Neurons Driven by Correlated Stochastic Input , 2002, Neural Computation.

[27]  Jaime de la Rocha,et al.  Supplementary Information for the article ‘ Correlation between neural spike trains increases with firing rate ’ , 2007 .

[28]  Gustavo Deco,et al.  Neural Network Mechanisms Underlying Stimulus Driven Variability Reduction , 2012, PLoS Comput. Biol..

[29]  A. Aertsen,et al.  Conditions for Propagating Synchronous Spiking and Asynchronous Firing Rates in a Cortical Network Model , 2008, The Journal of Neuroscience.

[30]  Stefan Rotter,et al.  Measurement of variability dynamics in cortical spike trains , 2008, Journal of Neuroscience Methods.

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

[32]  Sonja Grün,et al.  Noise Suppression and Surplus Synchrony by Coincidence Detection , 2012, PLoS Comput. Biol..

[33]  Prof. Dr. Dr. Valentino Braitenberg,et al.  Cortex: Statistics and Geometry of Neuronal Connectivity , 1998, Springer Berlin Heidelberg.

[34]  Nikos Yannaros ON COX PROCESSES AND GAMMA RENEWAL PROCESSES , 1988 .

[35]  D. Kaplan,et al.  Developing with BDNF: A Moving Experience , 2007, Neuron.

[36]  Néstor Parga,et al.  Auto- and crosscorrelograms for the spike response of leaky integrate-and-fire neurons with slow synapses. , 2006, Physical review letters.

[37]  Horace Barlow,et al.  What is the computational goal of the neocortex , 1994 .

[38]  Purvis Bedenbaugh,et al.  Multiunit Normalized Cross Correlation Differs from the Average Single-Unit Normalized Correlation , 1997, Neural Computation.

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

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

[41]  L. Abbott,et al.  Stimulus-dependent suppression of chaos in recurrent neural networks. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[42]  Moritz Helias,et al.  Correlations in spiking neuronal networks with distance dependent connections , 2009, Journal of Computational Neuroscience.

[43]  Brent Doiron,et al.  Theory of oscillatory firing induced by spatially correlated noise and delayed inhibitory feedback. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[44]  Jude F. Mitchell,et al.  Spatial Attention Decorrelates Intrinsic Activity Fluctuations in Macaque Area V4 , 2009, Neuron.

[45]  Ehud Zohary,et al.  Correlated neuronal discharge rate and its implications for psychophysical performance , 1994, Nature.

[46]  Moritz Helias,et al.  Structural Plasticity Controlled by Calcium Based Correlation Detection , 2008, Frontiers Comput. Neurosci..

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

[48]  Ad Aertsen,et al.  Physiology and Impact of Horizontal Connections in Rat Neocortex. , 2015, Cerebral cortex.

[49]  Mike W Oram,et al.  Visual stimulation decorrelates neuronal activity. , 2011, Journal of neurophysiology.

[50]  Moritz Helias,et al.  Neuroinformatics Original Research Article Pynest: a Convenient Interface to the Nest Simulator , 2022 .

[51]  Moritz Helias,et al.  Decorrelation of Neural-Network Activity by Inhibitory Feedback , 2012, PLoS Comput. Biol..

[52]  Sungho Hong,et al.  Single Neuron Firing Properties Impact Correlation-Based Population Coding , 2012, The Journal of Neuroscience.

[53]  Sonja Grün,et al.  CuBIC: cumulant based inference of higher-order correlations in massively parallel spike trains , 2009, Journal of Computational Neuroscience.

[54]  A. Litwin-Kumar,et al.  Slow dynamics and high variability in balanced cortical networks with clustered connections , 2012, Nature Neuroscience.

[55]  W. Gerstner,et al.  Optimal Control of Transient Dynamics in Balanced Networks Supports Generation of Complex Movements , 2014, Neuron.

[56]  Alison L. Barth,et al.  Experimental evidence for sparse firing in the neocortex , 2012, Trends in Neurosciences.

[57]  L.F. Abbott,et al.  Gating Multiple Signals through Detailed Balance of Excitation and Inhibition in Spiking Networks , 2009, Nature Neuroscience.

[58]  Brent Doiron,et al.  Oscillatory activity in electrosensory neurons increases with the spatial correlation of the stochastic input stimulus. , 2004, Physical review letters.

[59]  Wulfram Gerstner,et al.  SPIKING NEURON MODELS Single Neurons , Populations , Plasticity , 2002 .

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

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

[62]  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.

[63]  Markus Diesmann,et al.  Activity dynamics and propagation of synchronous spiking in locally connected random networks , 2003, Biological Cybernetics.

[64]  A. Aertsen,et al.  Beyond the Cortical Column: Abundance and Physiology of Horizontal Connections Imply a Strong Role for Inputs from the Surround , 2011, Front. Neurosci..

[65]  Néstor Parga,et al.  Theory of Input Spike Auto- and Cross-Correlations and Their Effect on the Response of Spiking Neurons , 2007, Neural Computation.

[66]  J. Assad,et al.  Beyond Poisson: Increased Spike-Time Regularity across Primate Parietal Cortex , 2009, Neuron.