The Influence of Synaptic Weight Distribution on Neuronal Population Dynamics

The manner in which different distributions of synaptic weights onto cortical neurons shape their spiking activity remains open. To characterize a homogeneous neuronal population, we use the master equation for generalized leaky integrate-and-fire neurons with shot-noise synapses. We develop fast semi-analytic numerical methods to solve this equation for either current or conductance synapses, with and without synaptic depression. We show that its solutions match simulations of equivalent neuronal networks better than those of the Fokker-Planck equation and we compute bounds on the network response to non-instantaneous synapses. We apply these methods to study different synaptic weight distributions in feed-forward networks. We characterize the synaptic amplitude distributions using a set of measures, called tail weight numbers, designed to quantify the preponderance of very strong synapses. Even if synaptic amplitude distributions are equated for both the total current and average synaptic weight, distributions with sparse but strong synapses produce higher responses for small inputs, leading to a larger operating range. Furthermore, despite their small number, such synapses enable the network to respond faster and with more stability in the face of external fluctuations.

[1]  N. Kampen,et al.  Stochastic processes in physics and chemistry , 1981 .

[2]  Márton Rózsa,et al.  Fluoxetine (Prozac) and Serotonin Act on Excitatory Synaptic Transmission to Suppress Single Layer 2/3 Pyramidal Neuron-Triggered Cell Assemblies in the Human Prefrontal Cortex , 2012, The Journal of Neuroscience.

[3]  T. Harkany,et al.  Pyramidal cell communication within local networks in layer 2/3 of rat neocortex , 2003, The Journal of physiology.

[4]  Bruce W. Knight,et al.  Dynamics of Encoding in Neuron Populations: Some General Mathematical Features , 2000, Neural Computation.

[5]  J. Deuchars,et al.  CA1 pyramidal to basket and bistratified cell EPSPs: dual intracellular recordings in rat hippocampal slices , 1998, The Journal of physiology.

[6]  Moritz Helias,et al.  Instantaneous Non-Linear Processing by Pulse-Coupled Threshold Units , 2010, PLoS Comput. Biol..

[7]  William R. Softky,et al.  Simple codes versus efficient codes , 1995, Current Opinion in Neurobiology.

[8]  M. J. Friedlander,et al.  The time course and amplitude of EPSPs evoked at synapses between pairs of CA3/CA1 neurons in the hippocampal slice , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  Lawrence Sirovich,et al.  Dynamics of Neuronal Populations: The Equilibrium Solution , 2000, SIAM J. Appl. Math..

[10]  Moritz Helias,et al.  Finite Post Synaptic Potentials Cause a Fast Neuronal Response , 2010, Front. Neurosci..

[11]  Benjamin Lindner,et al.  Method to calculate the moments of the membrane voltage in a model neuron driven by multiplicative filtered shot noise. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[12]  Moritz Helmstaedter,et al.  Monosynaptic connections between pairs of L5A pyramidal neurons in columns of juvenile rat somatosensory cortex. , 2008, Cerebral cortex.

[13]  Lawrence Sirovich,et al.  On the Simulation of Large Populations of Neurons , 2004, Journal of Computational Neuroscience.

[14]  Leslie G. Valiant,et al.  Circuits of the mind , 1994 .

[15]  Lawrence Sirovich,et al.  Dynamics of neuronal populations: eigenfunction theory; some solvable cases , 2003, Network.

[16]  Duane Q. Nykamp,et al.  A Population Density Approach That Facilitates Large-Scale Modeling of Neural Networks: Analysis and an Application to Orientation Tuning , 2004, Journal of Computational Neuroscience.

[17]  William Feller,et al.  On the integro-differential equations of purely discontinuous Markoff processes , 1940 .

[18]  N. Matsuki,et al.  Interpyramid spike transmission stabilizes the sparseness of recurrent network activity. , 2013, Cerebral cortex.

[19]  A. Kolmogoroff Über die analytischen Methoden in der Wahrscheinlichkeitsrechnung , 1931 .

[20]  Moritz Helias,et al.  Equilibrium and response properties of the integrate-and-fi re neuron in discrete time , 2022 .

[21]  W. Feller On the Theory of Stochastic Processes, with Particular Reference to Applications , 1949 .

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

[23]  P. J. Sjöström,et al.  Rate, Timing, and Cooperativity Jointly Determine Cortical Synaptic Plasticity , 2001, Neuron.

[24]  D. Sherrington Stochastic Processes in Physics and Chemistry , 1983 .

[25]  B. Barbour,et al.  Properties of Unitary Granule Cell→Purkinje Cell Synapses in Adult Rat Cerebellar Slices , 2002, The Journal of Neuroscience.

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

[27]  Anthony N. Burkitt,et al.  A Review of the Integrate-and-fire Neuron Model: I. Homogeneous Synaptic Input , 2006, Biological Cybernetics.

[28]  J. Nadal,et al.  Optimal Information Storage and the Distribution of Synaptic Weights Perceptron versus Purkinje Cell , 2004, Neuron.

[29]  W. John Wilbur,et al.  An analysis of Stein's model for stochastic neuronal excitation , 1982, Biological Cybernetics.

[30]  Csaba Varga,et al.  Complex Events Initiated by Individual Spikes in the Human Cerebral Cortex , 2008, PLoS biology.

[31]  Sen Song,et al.  Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS biology.

[32]  R. Stein A THEORETICAL ANALYSIS OF NEURONAL VARIABILITY. , 1965, Biophysical journal.

[33]  H. Markram,et al.  Redistribution of synaptic efficacy between neocortical pyramidal neurons , 1996, Nature.

[34]  Tomoki Fukai,et al.  Optimal spike-based communication in excitable networks with strong-sparse and weak-dense links , 2012, Scientific Reports.

[35]  J. Lübke,et al.  Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single ‘barrel’ of developing rat somatosensory cortex , 1999, The Journal of physiology.

[36]  R. Miles,et al.  Variation in strength of inhibitory synapses in the CA3 region of guinea‐pig hippocampus in vitro. , 1990, The Journal of physiology.

[37]  K. Stratford,et al.  Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  D. Hansel,et al.  How Spike Generation Mechanisms Determine the Neuronal Response to Fluctuating Inputs , 2003, The Journal of Neuroscience.

[39]  Stefan Mihalas,et al.  Self-organized criticality occurs in non-conservative neuronal networks during Up states , 2010, Nature physics.

[40]  H. Markram,et al.  Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. , 1997, The Journal of physiology.

[41]  Rupert Swarbrick,et al.  Firing-rate response of a neuron receiving excitatory and inhibitory synaptic shot noise. , 2010, Physical review letters.

[42]  Wulfram Gerstner,et al.  Statistics of subthreshold neuronal voltage fluctuations due to conductance-based synaptic shot noise. , 2006, Chaos.

[43]  A. Burkitt,et al.  Shot noise in the leaky integrate-and-fire neuron. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[44]  C. Petersen,et al.  The Excitatory Neuronal Network of the C2 Barrel Column in Mouse Primary Somatosensory Cortex , 2009, Neuron.