Mean-field analysis of selective persistent activity in presence of short-term synaptic depression

Mean-Field theory is extended to recurrent networks of spiking neurons endowed with short-term depression (STD) of synaptic transmission. The extension involves the use of the distribution of interspike intervals of an integrate-and-fire neuron receiving a Gaussian current, with a given mean and variance, in input. This, in turn, is used to obtain an accurate estimate of the resulting postsynaptic current in presence of STD. The stationary states of the network are obtained requiring self-consistency for the currents—those driving the emission processes and those generated by the emitted spikes. The model network stores in the distribution of two-state efficacies of excitatory-to-excitatory synapses, a randomly composed set of external stimuli. The resulting synaptic structure allows the network to exhibit selective persistent activity for each stimulus in the set. Theory predicts the onset of selective persistent, or working memory (WM) activity upon varying the constitutive parameters (e.g. potentiated/depressed long-term efficacy ratio, parameters associated with STD), and provides the average emission rates in the various steady states. Theoretical estimates are in remarkably good agreement with data “recorded” in computer simulations of the microscopic model.

[1]  J. Griffiths The Theory of Stochastic Processes , 1967 .

[2]  Henry C. Tuckwell,et al.  Introduction to theoretical neurobiology , 1988 .

[3]  D. Amit,et al.  Quantitative study of attractor neural networks retrieving at low spike rates: II. Low-rate retrieval in symmetric networks , 1991 .

[4]  Daniel J. Amit,et al.  Quantitative Study of Attractor Neural Network Retrieving at Low Spike Rates: I , 1991 .

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

[6]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

[7]  H. Markram,et al.  The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Nicolas Brunel,et al.  Dynamics of a recurrent network of spiking neurons before and following learning , 1997 .

[9]  S C Rao,et al.  Integration of what and where in the primate prefrontal cortex. , 1997, Science.

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

[11]  N Brunel,et al.  Slow stochastic Hebbian learning of classes of stimuli in a recurrent neural network. , 1998, Network.

[12]  S. Hestrin,et al.  Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex , 1998, Nature Neuroscience.

[13]  H. Markram,et al.  Differential signaling via the same axon of neocortical pyramidal neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Daniel J. Amit,et al.  Simulation in neurobiology: theory or experiment? , 1998, Trends in Neurosciences.

[15]  N. Brunel,et al.  Firing frequency of leaky intergrate-and-fire neurons with synaptic current dynamics. , 1998, Journal of theoretical biology.

[16]  Henry Markram,et al.  Neural Networks with Dynamic Synapses , 1998, Neural Computation.

[17]  J. A. Varela,et al.  Differential Depression at Excitatory and Inhibitory Synapses in Visual Cortex , 1999, The Journal of Neuroscience.

[18]  J. Leo van Hemmen,et al.  Short-Term Synaptic Plasticity and Network Behavior , 1999, Neural Computation.

[19]  X. Wang,et al.  Synaptic Basis of Cortical Persistent Activity: the Importance of NMDA Receptors to Working Memory , 1999, The Journal of Neuroscience.

[20]  R. Desimone,et al.  Responses of Macaque Perirhinal Neurons during and after Visual Stimulus Association Learning , 1999, The Journal of Neuroscience.

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

[22]  Davide Badoni,et al.  Spike-Driven Synaptic Plasticity: Theory, Simulation, VLSI Implementation , 2000, Neural Computation.

[23]  H. Markram,et al.  t Synchrony Generation in Recurrent Networks with Frequency-Dependent Synapses , 2000, The Journal of Neuroscience.

[24]  Misha Tsodyks,et al.  Chaos in neural networks with dynamic synapses , 2000, Neurocomputing.

[25]  G. Elston,et al.  Pyramidal Cells, Patches, and Cortical Columns: a Comparative Study of Infragranular Neurons in TEO, TE, and the Superior Temporal Polysensory Area of the Macaque Monkey , 2000, The Journal of Neuroscience.

[26]  P. Goldman-Rakic,et al.  Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. , 2000, Cerebral cortex.

[27]  Ruey-Beei Wu,et al.  Differential Signaling , 2000 .

[28]  T. Geisel,et al.  Pattern storage and processing in attractor networks with short-time synaptic dynamics , 2002, Network.

[29]  Hilbert J. Kappen,et al.  Associative Memory with Dynamic Synapses , 2002, Neural Computation.

[30]  D. Amit,et al.  Retrospective and prospective persistent activity induced by Hebbian learning in a recurrent cortical network , 2003, The European journal of neuroscience.

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

[32]  Daniel J. Amit,et al.  Spike-Driven Synaptic Dynamics Generating Working Memory States , 2003, Neural Computation.

[33]  D J Amit,et al.  Multiple-object working memory--a model for behavioral performance. , 2003, Cerebral cortex.

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

[35]  Gianluigi Mongillo,et al.  Selective delay activity in the cortex: phenomena and interpretation. , 2003, Cerebral cortex.

[36]  Nicolas Brunel,et al.  Dynamics and plasticity of stimulus-selective persistent activity in cortical network models. , 2003, Cerebral cortex.

[37]  P. Patie On some First Passage Time Problems Motivated by Financial Applications , 2004 .

[38]  N. Parga,et al.  Role of synaptic filtering on the firing response of simple model neurons. , 2004, Physical review letters.

[39]  Xiao-Jing Wang,et al.  Effects of Neuromodulation in a Cortical Network Model of Object Working Memory Dominated by Recurrent Inhibition , 2004, Journal of Computational Neuroscience.

[40]  Daniel J. Amit,et al.  Mean Field and Capacity in Realistic Networks of Spiking Neurons Storing Sparsely Coded Random Memories , 2004, Neural Computation.

[41]  Misha Tsodyks,et al.  Computation by Ensemble Synchronization in Recurrent Networks with Synaptic Depression , 2002, Journal of Computational Neuroscience.

[42]  Sandro Romani,et al.  Learning in realistic networks of spiking neurons and spike‐driven plastic synapses , 2005, The European journal of neuroscience.

[43]  Jianfeng Feng,et al.  Computational neuroscience , 1986, Behavioral and Brain Sciences.