Attractor Reliability Reveals Deterministic Structure in Neuronal Spike Trains

When periodic current is injected into an integrate-and-fire model neuron, the voltage as a function of time converges from different initial conditions to an attractor that produces reproducible sequences of spikes. The attractor reliability is a measure of the stability of spike trains against intrinsic noise and is quantified here as the inverse of the number of distinct spike trains obtained in response to repeated presentations of the same stimulus. High reliability characterizes neurons that can support a spike-time code, unlike neurons with discharges forming a renewal process (such as a Poisson process). These two classes of responses cannot be distinguished using measures based on the spike-time histogram, but they can be identified by the attractor dynamics of spike trains, as shown here using a new method for calculating the attractor reliability. We applied these methods to spike trains obtained from current injection into cortical neurons recorded in vitro. These spike trains did not form a renewal process and had a higher reliability compared to renewal-like processes with the same spike-time histogram.

[1]  Milton Abramowitz,et al.  Handbook of Mathematical Functions with Formulas, Graphs, and Mathematical Tables , 1964 .

[2]  R. Larsen An introduction to mathematical statistics and its applications / Richard J. Larsen, Morris L. Marx , 1986 .

[3]  C. Stevens,et al.  Origin of variability in quantal size in cultured hippocampal neurons and hippocampal slices. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[4]  William H. Press,et al.  Numerical recipes , 1990 .

[5]  C. Stevens,et al.  An evaluation of causes for unreliability of synaptic transmission. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[6]  T. Sejnowski,et al.  Reliability of spike timing in neocortical neurons. , 1995, Science.

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

[8]  J. Victor,et al.  Nature and precision of temporal coding in visual cortex: a metric-space analysis. , 1996, Journal of neurophysiology.

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

[10]  Maria V. Sanchez-Vives,et al.  Influence of low and high frequency inputs on spike timing in visual cortical neurons. , 1997, Cerebral cortex.

[11]  T. Sejnowski,et al.  Effects of cholinergic modulation on responses of neocortical neurons to fluctuating input. , 1997, Cerebral cortex.

[12]  B. Knight,et al.  The Power Ratio and the Interval Map: Spiking Models and Extracellular Recordings , 1998, The Journal of Neuroscience.

[13]  Neil Gershenfeld,et al.  The nature of mathematical modeling , 1998 .

[14]  Germán Mato,et al.  On Numerical Simulations of Integrate-and-Fire Neural Networks , 1998, Neural Computation.

[15]  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.

[16]  J. Kretzberg,et al.  Temporal precision of the encoding of motion information by visual interneurons , 1998, Current Biology.

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

[18]  R. Jensen Synchronization of randomly driven nonlinear oscillators , 1998 .

[19]  A. Zador Impact of synaptic unreliability on the information transmitted by spiking neurons. , 1998, Journal of neurophysiology.

[20]  J. D. Hunter,et al.  Resonance effect for neural spike time reliability. , 1998, Journal of neurophysiology.

[21]  B J Richmond,et al.  Stochastic nature of precisely timed spike patterns in visual system neuronal responses. , 1999, Journal of neurophysiology.

[22]  J. Kretzberg,et al.  Reliability of a Fly Motion-Sensitive Neuron Depends on Stimulus Parameters , 2000, The Journal of Neuroscience.

[23]  William Bialek,et al.  Synergy in a Neural Code , 2000, Neural Computation.

[24]  G A Cecchi,et al.  Noise in neurons is message dependent. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[25]  M C Eguia,et al.  Information transmission and recovery in neural communications channels. , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[26]  Rajesh P. N. Rao,et al.  Frequency dependence of spike timing reliability in cortical pyramidal cells and interneurons. , 2001, Journal of neurophysiology.

[27]  P H Tiesinga,et al.  Information transmission and recovery in neural communication channels revisited. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[28]  B. Kendall Nonlinear Dynamics and Chaos , 2001 .

[29]  M. Abeles,et al.  Detecting precise firing sequences in experimental data , 2001, Journal of Neuroscience Methods.

[30]  Paul H. E. Tiesinga,et al.  A New Correlation-Based Measure of Spike Timing Reliability , 2002, Neurocomputing.

[31]  Ernst Niebur,et al.  The Effects of Input Rate and Synchrony on a Coincidence Detector: Analytical Solution , 2003, Neural Computation.

[32]  Emmanuel Guigon,et al.  Reliability of Spike Timing Is a General Property of Spiking Model Neurons , 2003, Neural Computation.

[33]  Shigeru Shinomoto,et al.  Differences in Spiking Patterns Among Cortical Neurons , 2003, Neural Computation.

[34]  Martin Egelhaaf,et al.  Membrane Potential Fluctuations Determine the Precision of Spike Timing and Synchronous Activity: A Model Study , 2004, Journal of Computational Neuroscience.