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Science 21 March 1997: Vol. 275. no. 5307, pp. 1805 - 1808 DOI: 10.1126/science.275.5307.1805
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Reports
Reproducibility and Variability in Neural Spike Trains
Rob R. de Ruyter van Steveninck,
Geoffrey D. Lewen,
Steven P. Strong,
*
Roland Koberle,
William Bialek
To provide information about dynamic sensory stimuli, the pattern
of action potentials in spiking neurons must be variable. To ensure
reliability these variations must be related, reproducibly, to the
stimulus. For H1, a motion-sensitive neuron in the fly's visual
system, constant-velocity motion produces irregular spike firing
patterns, and spike counts typically have a variance comparable to the
mean, for cells in the mammalian cortex. But more natural, time-dependent input signals yield patterns of spikes that are much
more reproducible, both in terms of timing and of counting precision.
Variability and reproducibility are quantified with ideas from
information theory, and measured spike sequences in H1 carry more than
twice the amount of information they would if they followed the
variance-mean relation seen with constant inputs. Thus, models that may
accurately account for the neural response to static stimuli can
significantly underestimate the reliability of signal transfer under
more natural conditions.
R. R. de Ruyter van Steveninck, G. D. Lewen, S. P. Strong, W. Bialek,
NEC Research Institute, 4 Independence Way, Princeton, NJ 08540, USA.
R. Koberle, Department of Physics, Princeton University, Princeton, NJ
08544, and NEC Research Institute, 4 Independence Way, Princeton, NJ
08540, USA.
*
Present address: School of Natural Sciences, Institute for
Advanced Study, Olden Lane, Princeton, NJ 08540, USA.
Present address: Instituto de Física e Química
de São Carlos (IFQSC), Universidade de São Paolo, 13560 São Carlos SP, Brazil.
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| Full Text »
| PDF »
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| Abstract »
| Full Text »
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| Abstract »
| Full Text »
| PDF »
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| Abstract »
| Full Text »
| PDF »
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| Abstract »
| Full Text »
| PDF »
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| Abstract »
| Full Text »
| PDF »
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| Abstract »
| Full Text »
| PDF »
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| Abstract »
| Full Text »
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| Abstract »
| Full Text »
| PDF »
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- J. M. Samonds, J. D. Allison, H. A. Brown, and A. B. Bonds (2003)
J. Neurosci.
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| Abstract »
| Full Text »
| PDF »
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- N. C. Rust, S. R. Schultz, and J. A. Movshon (2002)
J. Neurosci.
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| Abstract »
| Full Text »
| PDF »
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- D. Zoccolan, G. Pinato, and V. Torre (2002)
J. Neurosci.
22, 10790-10800
| Abstract »
| Full Text »
| PDF »
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- P. Reinagel and R. C. Reid (2002)
J. Neurosci.
22, 6837-6841
| Abstract »
| Full Text »
| PDF »
- Natural Stimulation of the Nonclassical Receptive Field Increases Information Transmission Efficiency in V1.
- W. E. Vinje and J. L. Gallant (2002)
J. Neurosci.
22, 2904-2915
| Abstract »
| Full Text »
| PDF »
- Variability and Information in a Neural Code of the Cat Lateral Geniculate Nucleus.
- R. C. Liu, S. Tzonev, S. Rebrik, and K. D. Miller (2001)
J Neurophysiol
86, 2789-2806
| Abstract »
| Full Text »
| PDF »
- Consistency of Encoding in Monkey Visual Cortex.
- M. C. Wiener, M. W. Oram, Z. Liu, and B. J. Richmond (2001)
J. Neurosci.
21, 8210-8221
| Abstract »
| Full Text »
| PDF »
- Wavelets of Excitability in Sensory Neurons.
- J. Hasty, J. J. Collins, K. Wiesenfeld, and P. Grigg (2001)
J Neurophysiol
86, 2097-2101
| Abstract »
| Full Text »
| PDF »
- Recurrent Network Interactions Underlying Flow-Field Selectivity of Visual Interneurons.
- J. Haag and A. Borst (2001)
J. Neurosci.
21, 5685-5692
| Abstract »
| Full Text »
| PDF »
- Formal and Attribute-Specific Information in Primary Visual Cortex.
- D. S. Reich, F. Mechler, and J. D. Victor (2001)
J Neurophysiol
85, 305-318
| Abstract »
| Full Text »
| PDF »
- Information Theoretic Analysis of Pulmonary Stretch Receptor Spike Trains.
- R. F. Rogers, J. D. Runyan, A. G. Vaidyanathan, and J. S. Schwaber (2001)
J Neurophysiol
85, 448-461
| Abstract »
| Full Text »
| PDF »
- Reliability of a Fly Motion-Sensitive Neuron Depends on Stimulus Parameters.
- A.-K. Warzecha, J. Kretzberg, and M. Egelhaaf (2000)
J. Neurosci.
20, 8886-8896
| Abstract »
| Full Text »
| PDF »
- Temporal Coding of Visual Information in the Thalamus.
- P. Reinagel and R. C. Reid (2000)
J. Neurosci.
20, 5392-5400
| Abstract »
| Full Text »
| PDF »
- Robustness and Variability of Neuronal Coding by Amplitude-Sensitive Afferents in the Weakly Electric Fish Eigenmannia.
- G. Kreiman, R. Krahe, W. Metzner, C. Koch, and F. Gabbiani (2000)
J Neurophysiol
84, 189-204
| Abstract »
| Full Text »
| PDF »
- Population Reconstruction of the Locomotor Cycle From Interneuron Activity in the Mammalian Spinal Cord.
- M. C. Tresch and O. Kiehn (2000)
J Neurophysiol
83, 1972-1978
| Abstract »
| Full Text »
| PDF »
- Interspike Intervals, Receptive Fields, and Information Encoding in Primary Visual Cortex.
- D. S. Reich, F. Mechler, K. P. Purpura, and J. D. Victor (2000)
J. Neurosci.
20, 1964-1974
| Abstract »
| Full Text »
| PDF »
- Dynamic Control of Irregular Bursting in an Identified Neuron of an Oscillatory Circuit.
- R. C. Elson, R. Huerta, H. D. I. Abarbanel, M. I. Rabinovich, and A. I. Selverston (1999)
J Neurophysiol
82, 115-122
| Abstract »
| Full Text »
| PDF »
- Arginine Analogs Modify Signal Detection by Neurons in the Visual Cortex.
- P. Kara and M. J. Friedlander (1999)
J. Neurosci.
19, 5528-5548
| Abstract »
| Full Text »
| PDF »
- SI Neuron Response Variability Is Stimulus Tuned and NMDA Receptor Dependent.
- B. L. Whitsel, O. Favorov, K. A. Delemos, C.-J. Lee, M. Tommerdahl, G. K. Essick, and B. Nakhle (1999)
J Neurophysiol
81, 2988-3006
| Abstract »
| Full Text »
| PDF »
- Variability in Spike Trains During Constant and Dynamic Stimulation.
- A. Warzecha and M. Egelhaaf (1999)
Science
283, 1927-1930
| Abstract »
| Full Text »
- Cellular Mechanisms Contributing to Response Variability of Cortical Neurons In Vivo.
- R. Azouz and C. M. Gray (1999)
J. Neurosci.
19, 2209-2223
| Abstract »
| Full Text »
| PDF »
- Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type.
- G.-q. Bi and M.-m. Poo (1998)
J. Neurosci.
18, 10464-10472
| Abstract »
| Full Text »
| PDF »
- Resonance Effect for Neural Spike Time Reliability.
- J. D. Hunter, J. G. Milton, P. J. Thomas, and J. D. Cowan (1998)
J Neurophysiol
80, 1427-1438
| Abstract »
| Full Text »
| PDF »
- Multitasking in the Olfactory System: Context-Dependent Responses to Odors Reveal Dual GABA-Regulated Coding Mechanisms in Single Olfactory Projection Neurons.
- T. A. Christensen, B. R. Waldrop, and J. G. Hildebrand (1998)
J. Neurosci.
18, 5999-6008
| Abstract »
| Full Text »
| PDF »
- Spatiotemporal Structure of Cortical Activity: Properties and Behavioral Relevance.
- Y. Prut, E. Vaadia, H. Bergman, I. Haalman, H. Slovin, and M. Abeles (1998)
J Neurophysiol
79, 2857-2874
| Abstract »
| Full Text »
| PDF »
- Submicrosecond pacemaker precision is behaviorally modulated: The gymnotiform electromotor pathway.
- K. T. Moortgat, C. H. Keller, T. H. Bullock, and T. J. Sejnowski (1998)
PNAS
95, 4684-4689
| Abstract »
| Full Text »
| PDF »
- Refractoriness and Neural Precision.
- M. J. Berry II and M. Meister (1998)
J. Neurosci.
18, 2200-2211
| Abstract »
| Full Text »
| PDF »
- Coding Strategies in Monkey V1 and Inferior Temporal Cortices.
- E. D. Gershon, M. C. Wiener, P. E. Latham, and B. J. Richmond (1998)
J Neurophysiol
79, 1135-1144
| Abstract »
| Full Text »
| PDF »
- Impact of Synaptic Unreliability on the Information Transmitted by Spiking Neurons.
- A. Zador (1998)
J Neurophysiol
79, 1219-1229
| Abstract »
| Full Text »
| PDF »
- Variability and Correlated Noise in the Discharge of Neurons in Motor and Parietal Areas of the Primate Cortex.
- D. Lee, N. L. Port, W. Kruse, and A. P. Georgopoulos (1998)
J. Neurosci.
18, 1161-1170
| Abstract »
| Full Text »
| PDF »
- Relationship Between Repeated Measures of Hemodynamics, Muscle Sympathetic Nerve Activity, and Their Spectral Oscillations.
- P. van de Borne, N. Montano, B. Zimmerman, M. Pagani, and V. K. Somers (1997)
Circulation
96, 4326-4332
| Abstract »
| Full Text »
- The structure and precision of retinal spike trains.
- M. J. Berry, D. K. Warland, and M. Meister (1997)
PNAS
94, 5411-5416
| Abstract »
| Full Text »
| PDF »
- Noise in neurons is message dependent.
- G. A. Cecchi, M. Sigman, J.-M. Alonso, L. Martinez, D. R. Chialvo, and M. O. Magnasco (2000)
PNAS
97, 5557-5561
| Abstract »
| Full Text »
| PDF »
|
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