The impact of spike-frequency adaptation on balanced network dynamics

A dynamic balance between strong excitatory and inhibitory neuronal inputs is hypothesized to play a pivotal role in information processing in the brain. While there is evidence of the existence of a balanced operating regime in several cortical areas and idealized neuronal network models, it is important for the theory of balanced networks to be reconciled with more physiological neuronal modeling assumptions. In this work, we examine the impact of spike-frequency adaptation, observed widely across neurons in the brain, on balanced dynamics. We incorporate adaptation into binary and integrate-and-fire neuronal network models, analyzing the theoretical effect of adaptation in the large network limit and performing an extensive numerical investigation of the model adaptation parameter space. Our analysis demonstrates that balance is well preserved for moderate adaptation strength even if the entire network exhibits adaptation. In the common physiological case in which only excitatory neurons undergo adaptation, we show that the balanced operating regime in fact widens relative to the non-adaptive case. We hypothesize that spike-frequency adaptation may have been selected through evolution to robustly facilitate balanced dynamics across diverse cognitive operating states.

[1]  Guosong Liu,et al.  Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites , 2004, Nature Neuroscience.

[2]  L. Maler,et al.  Spike-Frequency Adaptation Separates Transient Communication Signals from Background Oscillations , 2005, The Journal of Neuroscience.

[3]  Edward T. Bullmore,et al.  Efficiency and Cost of Economical Brain Functional Networks , 2007, PLoS Comput. Biol..

[4]  Kenneth D. Miller,et al.  Physiological Gain Leads to High ISI Variability in a Simple Model of a Cortical Regular Spiking Cell , 1997, Neural Computation.

[5]  John Rinzel,et al.  A firing-rate model of spike-frequency adaptation in sinusoidally-driven thalamocortical relay neurons , 2001 .

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

[7]  David Cai,et al.  Dynamics of the exponential integrate-and-fire model with slow currents and adaptation , 2014, Journal of Computational Neuroscience.

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

[9]  Tsuyoshi Murata,et al.  {m , 1934, ACML.

[10]  Jeff Hasty,et al.  Delay-induced degrade-and-fire oscillations in small genetic circuits. , 2009, Physical review letters.

[11]  J. Movshon,et al.  Spike train encoding by regular-spiking cells of the visual cortex. , 1996, Journal of neurophysiology.

[12]  J. White,et al.  Epilepsy in Small-World Networks , 2004, The Journal of Neuroscience.

[13]  M. J. Richardson,et al.  Dynamics of populations and networks of neurons with voltage-activated and calcium-activated currents. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[14]  Zachary P. Kilpatrick,et al.  Sparse Gamma Rhythms Arising through Clustering in Adapting Neuronal Networks , 2011, PLoS Comput. Biol..

[15]  鈴木 増雄 Time-Dependent Statistics of the Ising Model , 1965 .

[16]  L. F. Abbott,et al.  Generating Coherent Patterns of Activity from Chaotic Neural Networks , 2009, Neuron.

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

[18]  Katsunori Kitano,et al.  Impact of slow K+ currents on spike generation can be described by an adaptive threshold model , 2016, Journal of Computational Neuroscience.

[19]  S. Nelson,et al.  Excitatory/Inhibitory Balance and Circuit Homeostasis in Autism Spectrum Disorders , 2015, Neuron.

[20]  Xiao-Jing Wang,et al.  Spike-Frequency Adaptation of a Generalized Leaky Integrate-and-Fire Model Neuron , 2004, Journal of Computational Neuroscience.

[21]  Arianna Maffei,et al.  Author ’ s Accepted Manuscript Neurophysiology and Regulation of the Balance Between Excitation and Inhibition in Neocortical CircuitsE / I Balance in Health and Disease , 2016 .

[22]  W. Senn,et al.  Neocortical pyramidal cells respond as integrate-and-fire neurons to in vivo-like input currents. , 2003, Journal of neurophysiology.

[23]  Tomoki Fukai,et al.  Balanced Excitatory and Inhibitory Inputs to Cortical Neurons Decouple Firing Irregularity from Rate Modulations , 2007, The Journal of Neuroscience.

[24]  Boris S. Gutkin,et al.  The effects of cholinergic neuromodulation on neuronal phase-response curves of modeled cortical neurons , 2009, Journal of Computational Neuroscience.

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

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

[27]  Cornelis J. Stam,et al.  Small-world and scale-free organization of voxel-based resting-state functional connectivity in the human brain , 2008, NeuroImage.

[28]  W. Gerstner,et al.  Parameter extraction and classification of three cortical neuron types reveals two distinct adaptation mechanisms. , 2012, Journal of neurophysiology.

[29]  A. Zador,et al.  Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex , 2003, Nature.

[30]  C. Koch,et al.  Multiple channels and calcium dynamics , 1989 .

[31]  S. Solla,et al.  Self-sustained activity in a small-world network of excitable neurons. , 2003, Physical review letters.

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

[33]  M. Scanziani,et al.  Instantaneous Modulation of Gamma Oscillation Frequency by Balancing Excitation with Inhibition , 2009, Neuron.

[34]  Jonathan Touboul,et al.  Dynamics and bifurcations of the adaptive exponential integrate-and-fire model , 2008, Biological Cybernetics.

[35]  D. McCormick,et al.  Turning on and off recurrent balanced cortical activity , 2003, Nature.

[36]  André Longtin,et al.  Linear versus nonlinear signal transmission in neuron models with adaptation currents or dynamic thresholds. , 2010, Journal of neurophysiology.

[37]  ErmentroutBard,et al.  The Effects of Spike Frequency Adaptation and Negative Feedback on the Synchronization of Neural Oscillators , 2001 .

[38]  D. A. Brown,et al.  Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone , 1980, Nature.

[39]  L. Pinneo On noise in the nervous system. , 1966, Psychological review.

[40]  R. Kobayashi The influence of firing mechanisms on gain modulation , 2008, 0807.1954.

[41]  Klaus Obermayer,et al.  How adaptation shapes spike rate oscillations in recurrent neuronal networks , 2012, Front. Comput. Neurosci..

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

[43]  D. Angelaki,et al.  A computational perspective on autism , 2015, Proceedings of the National Academy of Sciences.

[44]  Andreas V. M. Herz,et al.  A Universal Model for Spike-Frequency Adaptation , 2003, Neural Computation.

[45]  Boris S. Gutkin,et al.  The Effects of Spike Frequency Adaptation and Negative Feedback on the Synchronization of Neural Oscillators , 2001, Neural Computation.

[46]  David Cai,et al.  Sparsity and Compressed Coding in Sensory Systems , 2014, PLoS Comput. Biol..

[47]  S. N. Dorogovtsev,et al.  Evolution of networks , 2001, cond-mat/0106144.

[48]  Alan C. Evans,et al.  Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. , 2007, Cerebral cortex.

[49]  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.

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

[51]  M. London,et al.  Sensitivity to perturbations in vivo implies high noise and suggests rate coding in cortex , 2010, Nature.

[52]  Carl van Vreeswijk,et al.  Patterns of Synchrony in Neural Networks with Spike Adaptation , 2001, Neural Computation.

[53]  L. Maler,et al.  Suprathreshold stochastic firing dynamics with memory in P-type electroreceptors. , 2000, Physical review letters.

[54]  Ivanitskiĭ Ga,et al.  [Simulation of spontaneous discharge and short-term adaptation in acoustic nerve fibers]. , 1985 .

[55]  C. Gilbert Horizontal integration and cortical dynamics , 1992, Neuron.

[56]  Arenas,et al.  Self-organized criticality and synchronization in a lattice model of integrate-and-fire oscillators. , 1994, Physical review letters.

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

[58]  Moshe Abeles,et al.  On Embedding Synfire Chains in a Balanced Network , 2003, Neural Computation.

[59]  Olaf Sporns,et al.  Small worlds inside big brains , 2006, Proceedings of the National Academy of Sciences.

[60]  Christian K. Machens,et al.  Predictive Coding of Dynamical Variables in Balanced Spiking Networks , 2013, PLoS Comput. Biol..

[61]  P. Goldman-Rakic,et al.  Temporally irregular mnemonic persistent activity in prefrontal neurons of monkeys during a delayed response task. , 2003, Journal of neurophysiology.

[62]  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.

[63]  A. Treves Mean-field analysis of neuronal spike dynamics , 1993 .

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

[65]  R. Gao,et al.  Common mechanisms of excitatory and inhibitory imbalance in schizophrenia and autism spectrum disorders. , 2015, Current molecular medicine.

[66]  K. H. Britten,et al.  Responses of neurons in macaque MT to stochastic motion signals , 1993, Visual Neuroscience.

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

[68]  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.

[69]  W. Senn,et al.  Multiple time scales of temporal response in pyramidal and fast spiking cortical neurons. , 2006, Journal of neurophysiology.

[70]  S. Peron,et al.  Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron , 2009, Nature Neuroscience.

[71]  Katherine Whalley,et al.  Neural coding: Timing is key in the olfactory system , 2013, Nature Reviews Neuroscience.

[72]  E. Çinlar,et al.  On the Superposition of Point Processes , 1968 .

[73]  Christian K. Machens,et al.  Efficient codes and balanced networks , 2016, Nature Neuroscience.