Firing rate dynamics in recurrent spiking neural networks with intrinsic and network heterogeneity

Heterogeneity of neural attributes has recently gained a lot of attention and is increasing recognized as a crucial feature in neural processing. Despite its importance, this physiological feature has traditionally been neglected in theoretical studies of cortical neural networks. Thus, there is still a lot unknown about the consequences of cellular and circuit heterogeneity in spiking neural networks. In particular, combining network or synaptic heterogeneity and intrinsic heterogeneity has yet to be considered systematically despite the fact that both are known to exist and likely have significant roles in neural network dynamics. In a canonical recurrent spiking neural network model, we study how these two forms of heterogeneity lead to different distributions of excitatory firing rates. To analytically characterize how these types of heterogeneities affect the network, we employ a dimension reduction method that relies on a combination of Monte Carlo simulations and probability density function equations. We find that the relationship between intrinsic and network heterogeneity has a strong effect on the overall level of heterogeneity of the firing rates. Specifically, this relationship can lead to amplification or attenuation of firing rate heterogeneity, and these effects depend on whether the recurrent network is firing asynchronously or rhythmically firing. These observations are captured with the aforementioned reduction method, and furthermore simpler analytic descriptions based on this dimension reduction method are developed. The final analytic descriptions provide compact and descriptive formulas for how the relationship between intrinsic and network heterogeneity determines the firing rate heterogeneity dynamics in various settings.

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

[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]  Cheng Ly,et al.  Dynamics of Coupled Noisy Neural Oscillators with Heterogeneous Phase Resetting Curves , 2014, SIAM J. Appl. Dyn. Syst..

[4]  O. Bagasra,et al.  Proceedings of the National Academy of Sciences , 1914, Science.

[5]  Gustavo Deco,et al.  Stimulus-dependent variability and noise correlations in cortical MT neurons , 2013, Proceedings of the National Academy of Sciences.

[6]  A. Steger,et al.  Reliable Neuronal Systems: The Importance of Heterogeneity , 2013, PloS one.

[7]  Shreejoy J Tripathy,et al.  Intermediate intrinsic diversity enhances neural population coding , 2013, Proceedings of the National Academy of Sciences.

[8]  John A. White,et al.  Membrane Properties and the Balance between Excitation and Inhibition Control Gamma-Frequency Oscillations Arising from Feedback Inhibition , 2012, PLoS Comput. Biol..

[9]  D. Tranchina,et al.  Population density methods for large-scale modelling of neuronal networks with realistic synaptic kinetics: cutting the dimension down to size. , 2001, Network.

[10]  Xiao-Jing Wang Neurophysiological and computational principles of cortical rhythms in cognition. , 2010, Physiological reviews.

[11]  J F Mejias,et al.  Optimal heterogeneity for coding in spiking neural networks. , 2012, Physical review letters.

[12]  E. Haskell,et al.  Population density methods for large-scale modelling of neuronal networks with realistic synaptic kinetics: cutting the dimension down to size , 2001 .

[13]  Brent Doiron,et al.  Spatial Profile and Differential Recruitment of GABAB Modulate Oscillatory Activity in Auditory Cortex , 2009, The Journal of Neuroscience.

[14]  Nicolas Brunel,et al.  Synchronization properties of networks of electrically coupled neurons in the presence of noise and heterogeneities , 2009, Journal of Computational Neuroscience.

[15]  Leonard Maler,et al.  Neural heterogeneity and efficient population codes for communication signals. , 2010, Journal of neurophysiology.

[16]  André Longtin,et al.  Differential effects of excitatory and inhibitory heterogeneity on the gain and asynchronous state of sparse cortical networks , 2014, Front. Comput. Neurosci..

[17]  N. Urban,et al.  Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content , 2010, Nature Neuroscience.

[18]  G Bard Ermentrout,et al.  Intrinsic heterogeneity in oscillatory dynamics limits correlation-induced neural synchronization. , 2012, Journal of neurophysiology.

[19]  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.

[20]  A. Reyes,et al.  Spatial Profile of Excitatory and Inhibitory Synaptic Connectivity in Mouse Primary Auditory Cortex , 2012, The Journal of Neuroscience.

[21]  Srdjan Ostojic,et al.  Two types of asynchronous activity in networks of excitatory and inhibitory spiking neurons , 2014, Nature Neuroscience.

[22]  Kenneth D Harris,et al.  Stochastic transitions into silence cause noise correlations in cortical circuits , 2015, Proceedings of the National Academy of Sciences.

[23]  Cheng Ly,et al.  Population density methods for stochastic neurons with realistic synaptic kinetics: Firing rate dynamics and fast computational methods , 2006, Network.

[24]  Cheng Ly,et al.  Spike Train Statistics and Dynamics with Synaptic Input from any Renewal Process: A Population Density Approach , 2009, Neural Computation.

[25]  Nicolas Brunel,et al.  Analytical approximations of the firing rate of an adaptive exponential integrate-and-fire neuron in the presence of synaptic noise , 2014, Front. Comput. Neurosci..

[26]  E. Marder,et al.  Variability, compensation and homeostasis in neuron and network function , 2006, Nature Reviews Neuroscience.

[27]  Alex M Thomson,et al.  Binomial parameters differ across neocortical layers and with different classes of connections in adult rat and cat neocortex , 2007, Proceedings of the National Academy of Sciences.

[28]  Stefan Rotter,et al.  Impact of intrinsic biophysical diversity on the activity of spiking neurons , 2012, 1208.5350.

[29]  G. Buzsáki,et al.  Mechanisms of gamma oscillations. , 2012, Annual review of neuroscience.

[30]  Carson C. Chow Phase-locking in weakly heterogeneous neuronal networks , 1997, cond-mat/9709220.

[31]  Valentin Dragoi,et al.  Efficient coding in heterogeneous neuronal populations , 2008, Proceedings of the National Academy of Sciences.

[32]  Christopher J. Lee Open Peer Review by a Selected-Papers Network , 2011, Front. Comput. Neurosci..

[33]  J. Touboul,et al.  Heterogeneous connections induce oscillations in large-scale networks. , 2012, Physical review letters.

[34]  D. Parker Variable Properties in a Single Class of Excitatory Spinal Synapse , 2003, The Journal of Neuroscience.

[35]  Cheng Ly,et al.  A Principled Dimension-Reduction Method for the Population Density Approach to Modeling Networks of Neurons with Synaptic Dynamics , 2013, Neural Computation.

[36]  S. Strogatz,et al.  Stability of incoherence in a population of coupled oscillators , 1991 .

[37]  Cheng Ly,et al.  One-Dimensional Population Density Approaches to Recurrently Coupled Networks of Neurons with Noise , 2015, SIAM J. Appl. Math..

[38]  Alla Borisyuk,et al.  Fluctuation-driven rhythmogenesis in an excitatory neuronal network with slow adaptation , 2008, Journal of Computational Neuroscience.

[39]  E. Greisheimer,et al.  Physiology and Anatomy , 1934, The Indian Medical Gazette.

[40]  S. Schultz,et al.  Physiological Reviews , 1941 .

[41]  E. Marder Variability, compensation, and modulation in neurons and circuits , 2011, Proceedings of the National Academy of Sciences.

[42]  Duane Q. Nykamp,et al.  A Population Density Approach That Facilitates Large-Scale Modeling of Neural Networks: Extension to Slow Inhibitory Synapses , 2001, Neural Computation.

[43]  Nancy Kopell,et al.  Synchronization in Networks of Excitatory and Inhibitory Neurons with Sparse, Random Connectivity , 2003, Neural Computation.

[44]  Cheng Ly,et al.  Cellular and Circuit Mechanisms Maintain Low Spike Co-Variability and Enhance Population Coding in Somatosensory Cortex , 2012, Front. Comput. Neurosci..

[45]  Haim Sompolinsky,et al.  Implications of Neuronal Diversity on Population Coding , 2006, Neural Computation.

[46]  André Longtin,et al.  Learning Contrast-Invariant Cancellation of Redundant Signals in Neural Systems , 2013, PLoS Comput. Biol..

[47]  M. Scanziani,et al.  Equalizing Excitation-Inhibition Ratios across Visual Cortical Neurons , 2014, Nature.

[48]  Chris Eliasmith,et al.  The Competing Benefits of Noise and Heterogeneity in Neural Coding , 2014, Neural Computation.