Mechanism for neuronal spike generation by small and large ion channel clusters.

Neuronal action potentials are generated by clusters of ion channels between the Hillock and the first segment. If the clusters comprise a large number of sodium and potassium channels, action potentials are generated if the membrane potential exceeds a threshold of about -55 mV. Such behavior is well described by an excitable model such as, for example, the Hodgkin-Huxley equations. In this paper we show through stochastic modeling that if the size of the generating ion channel cluster is small, action potentials are generated regardless of whether the membrane potential is below or above the excitation threshold. Action potential generation is then determined by single-channel kinetics. We further show that this switch in generation mechanism manifests itself in peculiar statistical properties of the generated spike trains at small cluster sizes.

[1]  Peter Jung,et al.  Optimal sizes of ion channel clusters , 2001 .

[2]  Idan Segev,et al.  Ion Channel Stochasticity May Be Critical in Determining the Reliability and Precision of Spike Timing , 1998, Neural Computation.

[3]  J. Kurths,et al.  Coherence Resonance in a Noise-Driven Excitable System , 1997 .

[4]  Christof Koch,et al.  Subthreshold Voltage Noise Due to Channel Fluctuations in Active Neuronal Membranes , 2000, Journal of Computational Neuroscience.

[5]  H. Haken,et al.  Stochastic resonance without external periodic force. , 1993, Physical review letters.

[6]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[7]  Louis J. DeFelice,et al.  Chaotic states in a random world: Relationship between the nonlinear differential equations of excitability and the stochastic properties of ion channels , 1993 .

[8]  Christof Koch,et al.  Detecting and Estimating Signals in Noisy Cable Structures, I: Neuronal Noise Sources , 1999, Neural Computation.

[9]  Fox,et al.  Emergent collective behavior in large numbers of globally coupled independently stochastic ion channels. , 1994, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[10]  J. White,et al.  Channel noise in neurons , 2000, Trends in Neurosciences.

[11]  R. Fox Stochastic versions of the Hodgkin-Huxley equations. , 1997, Biophysical journal.

[12]  B. Sakmann,et al.  Single-channel currents recorded from membrane of denervated frog muscle fibres , 1976, Nature.

[13]  B. Hille Ionic channels of excitable membranes , 2001 .

[14]  I. Goychuk,et al.  Stochastic resonance as a collective property of ion channel assemblies , 2001, physics/0106036.

[15]  A. Longtin AUTONOMOUS STOCHASTIC RESONANCE IN BURSTING NEURONS , 1997 .

[16]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

[17]  L. Walløe,et al.  Firing behaviour in a stochastic nerve membrane model based upon the Hodgkin-Huxley equations. , 1979, Acta physiologica Scandinavica.

[18]  J. R. Clay,et al.  Relationship between membrane excitability and single channel open-close kinetics. , 1983, Biophysical journal.

[19]  Carson C. Chow,et al.  Spontaneous action potentials due to channel fluctuations. , 1996, Biophysical journal.