|
|
||||||||
Neural Computation, Vol 10, 1679-1703, Copyright © 1998 by The MIT Press
LETTERS |
Elad Schneidman, Barry Freedman and Idan Segev
The firing reliability and precision of an isopotential membrane patch consisting of a realistically large number of ion channels is investigated using a stochastic Hodgkin-Huxley (HH) model. In sharp contrast to the deterministic HH model, the biophysically inspired stochastic model reproduces qualitatively the different reliability and precision characteristics of spike firing in response to DC and fluctuating current input in neocortical neurons, as reported by Mainen & Sejnowski (1995). For DC inputs, spike timing is highly unreliable; the reliability and precision are significantly increased for fluctuating current input. This behavior is critically determined by the relatively small number of excitable channels that are opened near threshold for spike firing rather than by the total number of channels that exist in the membrane patch. Channel fluctuations, together with the inherent bistability in the HH equations, give rise to three additional experimentally observed phenomena: subthreshold oscillations in the membrane voltage for DC input, “spontaneous” spikes for subthreshold inputs, and “missing” spikes for suprathreshold inputs. We suggest that the noise inherent in the operation of ion channels enables neurons to act as “smart” encoders. Slowly varying, uncorrelated inputs are coded with low reliability and accuracy and, hence, the information about such inputs is encoded almost exclusively by the spike rate. On the other hand, correlated presynaptic activity produces sharp fluctuations in the input to the postsynaptic cell, which are then encoded with high reliability and accuracy. In this case, information about the input exists in the exact timing of the spikes. We conclude that channel stochasticity should be considered inrealistic models of neurons.
This article has been cited by other articles:
![]() |
D. Biron, S. Wasserman, J. H. Thomas, A. D. T. Samuel, and P. Sengupta An olfactory neuron responds stochastically to temperature and modulates Caenorhabditis elegans thermotactic behavior PNAS, August 5, 2008; 105(31): 11002 - 11007. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. R. Butson and G. A. Clark Random Noise Paradoxically Improves Light-Intensity Encoding in Hermissenda Photoreceptor Network J Neurophysiol, January 1, 2008; 99(1): 146 - 154. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. R. Butson and G. A. Clark Mechanisms of Noise-Induced Improvement in Light-Intensity Encoding in Hermissenda Photoreceptor Network J Neurophysiol, January 1, 2008; 99(1): 155 - 165. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Rowat Interspike Interval Statistics in the Stochastic Hodgkin-Huxley Model: Coexistence of Gamma Frequency Bursts and Highly Irregular Firing Neural Comput., May 1, 2007; 19(5): 1215 - 1250. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Radman, Y. Su, J. H. An, L. C. Parra, and M. Bikson Spike Timing Amplifies the Effect of Electric Fields on Neurons: Implications for Endogenous Field Effects J. Neurosci., March 14, 2007; 27(11): 3030 - 3036. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Paydarfar, D. B. Forger, and J. R. Clay Noisy Inputs and the Induction of On-Off Switching Behavior in a Neuronal Pacemaker J Neurophysiol, December 1, 2006; 96(6): 3338 - 3348. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. V. M. Herz, T. Gollisch, C. K. Machens, and D. Jaeger Modeling single-neuron dynamics and computations: a balance of detail and abstraction. Science, October 6, 2006; 314(5796): 80 - 85. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. D. Dorval The Rhythmic Consequences of Ion Channel Stochasticity Neuroscientist, October 1, 2006; 12(5): 442 - 448. [Abstract] [PDF] |
||||
![]() |
J. X. Gittelman and B. L Tempel Kv1.1-Containing Channels Are Critical for Temporal Precision During Spike Initiation J Neurophysiol, September 1, 2006; 96(3): 1203 - 1214. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. P. Billimoria, R. A. DiCaprio, J. T. Birmingham, L. F. Abbott, and E. Marder Neuromodulation of spike-timing precision in sensory neurons. J. Neurosci., May 31, 2006; 26(22): 5910 - 5919. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. H. P. Kole, S. Hallermann, and G. J. Stuart Single Ih Channels in Pyramidal Neuron Dendrites: Properties, Distribution, and Impact on Action Potential Output J. Neurosci., February 8, 2006; 26(6): 1677 - 1687. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. K. Dhingra, M. A. Freed, and R. G. Smith Voltage-Gated Sodium Channels Improve Contrast Sensitivity of a Retinal Ganglion Cell J. Neurosci., August 31, 2005; 25(35): 8097 - 8103. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. V. Carelli, M. B. Reyes, J. C. Sartorelli, and R. D. Pinto Whole Cell Stochastic Model Reproduces the Irregularities Found in the Membrane Potential of Bursting Neurons J Neurophysiol, August 1, 2005; 94(2): 1169 - 1179. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. A Jacobson, K. Diba, A. Yaron-Jakoubovitch, Y. Oz, C. Koch, I. Segev, and Y. Yarom Subthreshold voltage noise of rat neocortical pyramidal neurones J. Physiol., April 1, 2005; 564(1): 145 - 160. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Diba, H. A. Lester, and C. Koch Intrinsic Noise in Cultured Hippocampal Neurons: Experiment and Modeling J. Neurosci., October 27, 2004; 24(43): 9723 - 9733. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Tateno, A. Harsch, and H. P. C. Robinson Threshold Firing Frequency-Current Relationships of Neurons in Rat Somatosensory Cortex: Type 1 and Type 2 Dynamics J Neurophysiol, October 1, 2004; 92(4): 2283 - 2294. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Balu, P. Larimer, and B. W. Strowbridge Phasic Stimuli Evoke Precisely Timed Spikes in Intermittently Discharging Mitral Cells J Neurophysiol, August 1, 2004; 92(2): 743 - 753. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. K. Dhingra and R. G. Smith Spike Generator Limits Efficiency of Information Transfer in a Retinal Ganglion Cell J. Neurosci., March 24, 2004; 24(12): 2914 - 2922. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. Axmacher and R. Miles Intrinsic cellular currents and the temporal precision of EPSP-action potential coupling in CA1 pyramidal cells J. Physiol., March 15, 2004; 555(3): 713 - 725. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. A. y Arcas, A. L. Fairhall, and W. Bialek Computation in a Single Neuron: Hodgkin and Huxley Revisited Neural Comput., August 1, 2003; 15(8): 1715 - 1749. [Abstract] [Full Text] |
||||
![]() |
L. Cathala, S. Brickley, S. Cull-Candy, and M. Farrant Maturation of EPSCs and Intrinsic Membrane Properties Enhances Precision at a Cerebellar Synapse J. Neurosci., July 9, 2003; 23(14): 6074 - 6085. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. D. Hunter and J. G. Milton Amplitude and Frequency Dependence of Spike Timing: Implications for Dynamic Regulation J Neurophysiol, July 1, 2003; 90(1): 387 - 394. [Abstract] [Full Text] [PDF] |
||||
![]() |
M.C.W. van Rossum, B. J. O'Brien, and R. G. Smith Effects of Noise on the Spike Timing Precision of Retinal Ganglion Cells J Neurophysiol, May 1, 2003; 89(5): 2406 - 2419. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. W. Shuai and P. Jung Optimal ion channel clustering for intracellular calcium signaling PNAS, January 21, 2003; 100(2): 506 - 510. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. S. Haas and J. A. White Frequency Selectivity of Layer II Stellate Cells in the Medial Entorhinal Cortex J Neurophysiol, November 1, 2002; 88(5): 2422 - 2429. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Feng and G. Li Impact of Geometrical Structures on the Output of Neuronal Models: A Theoretical and Numerical Analysis Neural Comput., March 1, 2002; 14(3): 621 - 640. [Abstract] [Full Text] |
||||
![]() |
A. Manwani, P. N. Steinmetz, and C. Koch The Impact of Spike Timing Variability on the Signal-Encoding Performance of Neural Spiking Models Neural Comput., February 1, 2002; 14(2): 347 - 367. [Abstract] [Full Text] [PDF] |
||||
![]() |
J.-M. Fellous, A. R. Houweling, R. H. Modi, R.P.N. Rao, P.H.E. Tiesinga, and T. J. Sejnowski Frequency Dependence of Spike Timing Reliability in Cortical Pyramidal Cells and Interneurons J Neurophysiol, April 1, 2001; 85(4): 1782 - 1787. [Abstract] [Full Text] [PDF] |
||||
![]() |
I. Segev and M. London Untangling Dendrites with Quantitative Models Science, October 27, 2000; 290(5492): 744 - 750. [Abstract] [Full Text] |
||||
![]() |
A. Manwani and C. Koch Detecting and Estimating Signals in Noisy Cable Structures, I: Neuronal Noise Sources Neural Comput., November 15, 1999; 11(8): 1797 - 1829. [Abstract] [Full Text] |
||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| J COGNITIVE NEUROSCIENCE | NEURAL COMPUTATION | MIT PRESS JOURNALS |