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The Journal of Neuroscience, May 15, 1998, 18(10):3870-3896
The Variable Discharge of Cortical Neurons: Implications for
Connectivity, Computation, and Information Coding
Michael N.
Shadlen1 and
William T.
Newsome2
1 Department of Physiology and Biophysics and Regional
Primate Research Center, University of Washington, Seattle, Washington
98195-7290, and 2 Howard Hughes Medical Institute and
Department of Neurobiology, Stanford University School of Medicine,
Stanford, California 94305
Cortical neurons exhibit tremendous variability in the number and
temporal distribution of spikes in their discharge patterns. Furthermore, this variability appears to be conserved over large regions of the cerebral cortex, suggesting that it is neither reduced
nor expanded from stage to stage within a processing pathway. To
investigate the principles underlying such statistical homogeneity, we
have analyzed a model of synaptic integration incorporating a highly
simplified integrate and fire mechanism with decay. We analyzed a
"high-input regime" in which neurons receive hundreds of excitatory
synaptic inputs during each interspike interval. To produce a graded
response in this regime, the neuron must balance excitation with
inhibition. We find that a simple integrate and fire mechanism with
balanced excitation and inhibition produces a highly variable
interspike interval, consistent with experimental data. Detailed
information about the temporal pattern of synaptic inputs cannot be
recovered from the pattern of output spikes, and we infer that cortical
neurons are unlikely to transmit information in the temporal pattern of
spike discharge. Rather, we suggest that quantities are represented as
rate codes in ensembles of 50-100 neurons. These column-like ensembles
tolerate large fractions of common synaptic input and yet covary only
weakly in their spike discharge. We find that an ensemble of 100 neurons provides a reliable estimate of rate in just one interspike
interval (10-50 msec). Finally, we derived an expression for the
variance of the neural spike count that leads to a stable propagation
of signal and noise in networks of neurons that is, conditions that do
not impose an accumulation or diminution of noise. The solution implies that single neurons perform simple algebra resembling averaging, and
that more sophisticated computations arise by virtue of the anatomical
convergence of novel combinations of inputs to the cortical column from
external sources.
Key words:
noise; rate code; temporal coding; correlation; interspike interval; spike count variance; response variability; visual
cortex; synaptic integration; neural model
Copyright © 1998 Society for Neuroscience 0270-6474/98/18103870-27$05.00/0
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R. E. Kass, V. Ventura, and E. N. Brown
Statistical Issues in the Analysis of Neuronal Data
J Neurophysiol,
July 1, 2005;
94(1):
8 - 25.
[Abstract]
[Full Text]
[PDF]
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E. S. Frechette, A. Sher, M. I. Grivich, D. Petrusca, A. M. Litke, and E. J. Chichilnisky
Fidelity of the Ensemble Code for Visual Motion in Primate Retina
J Neurophysiol,
July 1, 2005;
94(1):
119 - 135.
[Abstract]
[Full Text]
[PDF]
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J. A. Henrie and R. Shapley
LFP Power Spectra in V1 Cortex: The Graded Effect of Stimulus Contrast
J Neurophysiol,
July 1, 2005;
94(1):
479 - 490.
[Abstract]
[Full Text]
[PDF]
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S. Shinomoto, Y. Miyazaki, H. Tamura, and I. Fujita
Regional and Laminar Differences in In Vivo Firing Patterns of Primate Cortical Neurons
J Neurophysiol,
July 1, 2005;
94(1):
567 - 575.
[Abstract]
[Full Text]
[PDF]
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S. R. Williams
Encoding and Decoding of Dendritic Excitation during Active States in Pyramidal Neurons
J. Neurosci.,
June 22, 2005;
25(25):
5894 - 5902.
[Abstract]
[Full Text]
[PDF]
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R. Schaette, T. Gollisch, and A. V. M. Herz
Spike-Train Variability of Auditory Neurons In Vivo: Dynamic Responses Follow Predictions From Constant Stimuli
J Neurophysiol,
June 1, 2005;
93(6):
3270 - 3281.
[Abstract]
[Full Text]
[PDF]
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M. Raffi and R. M. Siegel
Functional Architecture of Spatial Attention in the Parietal Cortex of the Behaving Monkey
J. Neurosci.,
May 25, 2005;
25(21):
5171 - 5186.
[Abstract]
[Full Text]
[PDF]
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M. A. Lebedev, J. M. Carmena, J. E. O'Doherty, M. Zacksenhouse, C. S. Henriquez, J. C. Principe, and M. A. L. Nicolelis
Cortical Ensemble Adaptation to Represent Velocity of an Artificial Actuator Controlled by a Brain-Machine Interface
J. Neurosci.,
May 11, 2005;
25(19):
4681 - 4693.
[Abstract]
[Full Text]
[PDF]
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D. Cai, A. V. Rangan, and D. W. McLaughlin
Architectural and synaptic mechanisms underlying coherent spontaneous activity in V1
PNAS,
April 19, 2005;
102(16):
5868 - 5873.
[Abstract]
[Full Text]
[PDF]
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A. Kohn and M. A. Smith
Stimulus Dependence of Neuronal Correlation in Primary Visual Cortex of the Macaque
J. Neurosci.,
April 6, 2005;
25(14):
3661 - 3673.
[Abstract]
[Full Text]
[PDF]
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S. Hill and G. Tononi
Modeling Sleep and Wakefulness in the Thalamocortical System
J Neurophysiol,
March 1, 2005;
93(3):
1671 - 1698.
[Abstract]
[Full Text]
[PDF]
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E. Hitt
Inaugural Article: Biography of William T. Newsome
PNAS,
January 18, 2005;
102(3):
521 - 523.
[Full Text]
[PDF]
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D. B. Katz
The Many Flavors of Temporal Coding in Gustatory Cortex
Chem Senses,
January 1, 2005;
30(suppl_1):
i80 - i81.
[Full Text]
[PDF]
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J. Hegde and D. C. Van Essen
Temporal Dynamics of Shape Analysis in Macaque Visual Area V2
J Neurophysiol,
November 1, 2004;
92(5):
3030 - 3042.
[Abstract]
[Full Text]
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J. B. Demb, P. Sterling, and M. A. Freed
How Retinal Ganglion Cells Prevent Synaptic Noise From Reaching the Spike Output
J Neurophysiol,
October 1, 2004;
92(4):
2510 - 2519.
[Abstract]
[Full Text]
[PDF]
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S. Tanabe, K. Umeda, and I. Fujita
Rejection of False Matches for Binocular Correspondence in Macaque Visual Cortical Area V4
J. Neurosci.,
September 15, 2004;
24(37):
8170 - 8180.
[Abstract]
[Full Text]
[PDF]
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E. Garcia-Perez, D. Zoccolan, G. Pinato, and V. Torre
Dynamics and Reproducibility of a Moderately Complex Sensory-Motor Response in the Medicinal Leech
J Neurophysiol,
September 1, 2004;
92(3):
1783 - 1795.
[Abstract]
[Full Text]
[PDF]
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M. R. Deweese and A. M. Zador
Shared and Private Variability in the Auditory Cortex
J Neurophysiol,
September 1, 2004;
92(3):
1840 - 1855.
[Abstract]
[Full Text]
[PDF]
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V. J. Uzzell and E. J. Chichilnisky
Precision of Spike Trains in Primate Retinal Ganglion Cells
J Neurophysiol,
August 1, 2004;
92(2):
780 - 789.
[Abstract]
[Full Text]
[PDF]
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M. Giugliano, P. Darbon, M. Arsiero, H.-R. Luscher, and J. Streit
Single-Neuron Discharge Properties and Network Activity in Dissociated Cultures of Neocortex
J Neurophysiol,
August 1, 2004;
92(2):
977 - 996.
[Abstract]
[Full Text]
[PDF]
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C. L. Passaglia and J. B. Troy
Impact of Noise on Retinal Coding of Visual Signals
J Neurophysiol,
August 1, 2004;
92(2):
1023 - 1033.
[Abstract]
[Full Text]
[PDF]
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C. C. Horn, Y. Zhurov, I. V. Orekhova, A. Proekt, I. Kupfermann, K. R. Weiss, and V. Brezina
Cycle-to-Cycle Variability of Neuromuscular Activity in Aplysia Feeding Behavior
J Neurophysiol,
July 1, 2004;
92(1):
157 - 180.
[Abstract]
[Full Text]
[PDF]
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P. Petersson, M. Granmo, and J. Schouenborg
Properties of an Adult Spinal Sensorimotor Circuit Shaped Through Early Postnatal Experience
J Neurophysiol,
July 1, 2004;
92(1):
280 - 288.
[Abstract]
[Full Text]
[PDF]
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J. Perez-Orive, M. Bazhenov, and G. Laurent
Intrinsic and Circuit Properties Favor Coincidence Detection for Decoding Oscillatory Input
J. Neurosci.,
June 30, 2004;
24(26):
6037 - 6047.
[Abstract]
[Full Text]
[PDF]
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W. J. Kargo and D. A. Nitz
Improvements in the Signal-to-Noise Ratio of Motor Cortex Cells Distinguish Early versus Late Phases of Motor Skill Learning
J. Neurosci.,
June 16, 2004;
24(24):
5560 - 5569.
[Abstract]
[Full Text]
[PDF]
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