 |
Previous Article | Next Article 
The Journal of Neuroscience, March 15, 1998, 18(6):2200-2211
Refractoriness and Neural Precision
Michael J.
Berry II and
Markus
Meister
Department of Molecular and Cellular Biology, Harvard University,
Cambridge, Massachusetts 02138
The response of a spiking neuron to a stimulus is often
characterized by its time-varying firing rate, estimated from a
histogram of spike times. If the cell's firing probability in each
small time interval depends only on this firing rate, one predicts a highly variable response to repeated trials, whereas many neurons show
much greater fidelity. Furthermore, the neuronal membrane is refractory
immediately after a spike, so that the firing probability depends not
only on the stimulus but also on the preceding spike train. To connect
these observations, we investigated the relationship between the
refractory period of a neuron and its firing precision. The light
response of retinal ganglion cells was modeled as probabilistic firing
combined with a refractory period: the instantaneous firing rate is the
product of a "free firing rate," which depends only on the
stimulus, and a "recovery function," which depends only on the time
since the last spike. This recovery function vanishes for an absolute
refractory period and then gradually increases to unity. In
simulations, longer refractory periods were found to make the response
more reproducible, eventually matching the precision of measured spike
trains. Refractoriness, although often thought to limit the performance
of neurons, may in fact benefit neuronal reliability. The underlying
free firing rate derived by allowing for the refractory period often
exceeded the observed firing rate by an order of magnitude and was
found to convey information about the stimulus over a much wider
dynamic range. Thus, the free firing rate may be the preferred variable
for describing the response of a spiking neuron.
Key words:
neural coding; retinal ganglion cell; spike generator; refractory period; reproducibility; Poisson process
Copyright © 1998 Society for Neuroscience 0270-6474/98/1862200-12$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
R. T. Kanichay and R. A. Silver
Synaptic and Cellular Properties of the Feedforward Inhibitory Circuit within the Input Layer of the Cerebellar Cortex
J. Neurosci.,
September 3, 2008;
28(36):
8955 - 8967.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Sekirnjak, P. Hottowy, A. Sher, W. Dabrowski, A. M. Litke, and E. J. Chichilnisky
High-Resolution Electrical Stimulation of Primate Retina for Epiretinal Implant Design
J. Neurosci.,
April 23, 2008;
28(17):
4446 - 4456.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. D. Kumbhani, M. J. Nolt, and L. A. Palmer
Precision, Reliability, and Information-Theoretic Analysis of Visual Thalamocortical Neurons
J Neurophysiol,
November 1, 2007;
98(5):
2647 - 2663.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. A. Montemurro, S. Panzeri, M. Maravall, A. Alenda, M. R. Bale, M. Brambilla, and R. S. Petersen
Role of Precise Spike Timing in Coding of Dynamic Vibrissa Stimuli in Somatosensory Thalamus
J Neurophysiol,
October 1, 2007;
98(4):
1871 - 1882.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. A. DiCaprio, C. P. Billimoria, and B. Ch. Ludwar
Information Rate and Spike-Timing Precision of Proprioceptive Afferents
J Neurophysiol,
September 1, 2007;
98(3):
1706 - 1717.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. S. Gaudry and P. Reinagel
Benefits of Contrast Normalization Demonstrated in Neurons and Model Cells
J. Neurosci.,
July 25, 2007;
27(30):
8071 - 8079.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Shlens, M. B. Kennel, H. D. I. Abarbanel, and E. J. Chichilnisky
Estimating information rates with confidence intervals in neural spike trains.
Neural Comput.,
July 1, 2007;
19(7):
1683 - 1719.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Avissar, A. C. Furman, J. C. Saunders, and T. D. Parsons
Adaptation Reduces Spike-Count Reliability, But Not Spike-Timing Precision, of Auditory Nerve Responses
J. Neurosci.,
June 13, 2007;
27(24):
6461 - 6472.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. C. Lee and A. T. Ishida
Ih Without Kir in Adult Rat Retinal Ganglion Cells
J Neurophysiol,
May 1, 2007;
97(5):
3790 - 3799.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A.-M. M. Oswald, B. Doiron, and L. Maler
Interval Coding. I. Burst Interspike Intervals as Indicators of Stimulus Intensity
J Neurophysiol,
April 1, 2007;
97(4):
2731 - 2743.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. D. Victor, E. M. Blessing, J. D. Forte, P. Buzas, and P. R. Martin
Response variability of marmoset parvocellular neurons
J. Physiol.,
February 15, 2007;
579(1):
29 - 51.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Wang, R. Narayan, G. Grana, M. Shamir, and K. Sen
Cortical Discrimination of Complex Natural Stimuli: Can Single Neurons Match Behavior?
J. Neurosci.,
January 17, 2007;
27(3):
582 - 589.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Greschner, A. Thiel, J. Kretzberg, and J. Ammermuller
Complex Spike-Event Pattern of Transient ON-OFF Retinal Ganglion Cells
J Neurophysiol,
December 1, 2006;
96(6):
2845 - 2856.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Paninski
The Spike-Triggered Average of the Integrate-and-Fire Cell Driven by Gaussian White Noise.
Neural Comput.,
November 1, 2006;
18(11):
2592 - 2616.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. R. Townsend, L. Paninski, and R. N. Lemon
Linear Encoding of Muscle Activity in Primary Motor Cortex and Cerebellum
J Neurophysiol,
November 1, 2006;
96(5):
2578 - 2592.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. L. Fairhall, C. A. Burlingame, R. Narasimhan, R. A. Harris, J. L. Puchalla, and M. J. Berry II
Selectivity for Multiple Stimulus Features in Retinal Ganglion Cells
J Neurophysiol,
November 1, 2006;
96(5):
2724 - 2738.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Schein and K. M. Ahmad
Efficiency of Synaptic Transmission of Single-Photon Events from Rod Photoreceptor to Rod Bipolar Dendrite
Biophys. J.,
November 1, 2006;
91(9):
3257 - 3267.
[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. M. Churchland, B. M. Yu, S. I. Ryu, G. Santhanam, and K. V. Shenoy
Neural variability in premotor cortex provides a signature of motor preparation.
J. Neurosci.,
April 5, 2006;
26(14):
3697 - 3712.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Schein and K. M. Ahmad
A Clockwork Hypothesis: Synaptic Release by Rod Photoreceptors Must Be Regular
Biophys. J.,
December 1, 2005;
89(6):
3931 - 3949.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. W. Pillow, L. Paninski, V. J. Uzzell, E. P. Simoncelli, and E. J. Chichilnisky
Prediction and Decoding of Retinal Ganglion Cell Responses with a Probabilistic Spiking Model
J. Neurosci.,
November 23, 2005;
25(47):
11003 - 11013.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Narayan, A. Ergun, and K. Sen
Delayed Inhibition in Cortical Receptive Fields and the Discrimination of Complex Stimuli
J Neurophysiol,
October 1, 2005;
94(4):
2970 - 2975.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. A. Freed
Quantal Encoding of Information in a Retinal Ganglion Cell
J Neurophysiol,
August 1, 2005;
94(2):
1048 - 1056.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Zsiros and S. Hestrin
Background Synaptic Conductance and Precision of EPSP-Spike Coupling at Pyramidal Cells
J Neurophysiol,
June 1, 2005;
93(6):
3248 - 3256.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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]
|
 |
|

|
 |

|
 |
 
E. E. Thomson and W. B. Kristan
Quantifying Stimulus Discriminability: A Comparison of Information Theory and Ideal Observer Analysis
Neural Comput.,
April 1, 2005;
17(4):
741 - 778.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. K Powers, Y Dai, B. M Bell, D. B Percival, and M. D Binder
Contributions of the input signal and prior activation history to the discharge behaviour of rat motoneurones
J. Physiol.,
February 1, 2005;
562(3):
707 - 724.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Paninski, J. W. Pillow, and E. P. Simoncelli
Maximum Likelihood Estimation of a Stochastic Integrate-and-Fire Neural Encoding Model
Neural Comput.,
December 1, 2004;
16(12):
2533 - 2561.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. W. Wheeler, P. H. M. Kullmann, and J. P. Horn
Estimating Use-Dependent Synaptic Gain in Autonomic Ganglia by Computational Simulation and Dynamic-Clamp Analysis
J Neurophysiol,
November 1, 2004;
92(5):
2659 - 2671.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
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]
|
 |
|

|
 |

|
 |
 
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]
|
 |
|

|
 |

|
 |
 
R. Dawkins and W. F. Sewell
Afferent Synaptic Transmission in a Hair Cell Organ: Pharmacological and Physiological Analysis of the Role of the Extended Refractory Period
J Neurophysiol,
August 1, 2004;
92(2):
1105 - 1115.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. S. Goldman
Enhancement of Information Transmission Efficiency by Synaptic Failures
Neural Comput.,
June 1, 2004;
16(6):
1137 - 1162.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J.-M. Fellous, P. H. E. Tiesinga, P. J. Thomas, and T. J. Sejnowski
Discovering Spike Patterns in Neuronal Responses
J. Neurosci.,
March 24, 2004;
24(12):
2989 - 3001.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. L. Passaglia and J. B. Troy
Information Transmission Rates of Cat Retinal Ganglion Cells
J Neurophysiol,
March 1, 2004;
91(3):
1217 - 1229.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Kara and R. C. Reid
Efficacy of Retinal Spikes in Driving Cortical Responses
J. Neurosci.,
September 17, 2003;
23(24):
8547 - 8557.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. R. DeWeese, M. Wehr, and A. M. Zador
Binary Spiking in Auditory Cortex
J. Neurosci.,
August 27, 2003;
23(21):
7940 - 7949.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. J. Chichilnisky and R. S. Kalmar
Temporal Resolution of Ensemble Visual Motion Signals in Primate Retina
J. Neurosci.,
July 30, 2003;
23(17):
6681 - 6689.
[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]
|
 |
|

|
 |

|
 |
 
L. Noonan, B. Doiron, C. Laing, A. Longtin, and R. W. Turner
A Dynamic Dendritic Refractory Period Regulates Burst Discharge in the Electrosensory Lobe of Weakly Electric Fish
J. Neurosci.,
February 15, 2003;
23(4):
1524 - 1534.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Brette and E. Guigon
Reliability of Spike Timing Is a General Property of Spiking Model Neurons
Neural Comput.,
February 1, 2003;
15(2):
279 - 308.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Panzeri, F. Petroni, R. S. Petersen, and M. E. Diamond
Decoding Neuronal Population Activity in Rat Somatosensory Cortex: Role of Columnar Organization
Cereb Cortex,
January 1, 2003;
13(1):
45 - 52.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. L. Oshinsky and R. R. Hoy
Physiology of the Auditory Afferents in an Acoustic Parasitoid Fly
J. Neurosci.,
August 15, 2002;
22(16):
7254 - 7263.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Brandman and M. E. Nelson
A Simple Model of Long-Term Spike Train Regularization
Neural Comput.,
July 1, 2002;
14(7):
1575 - 1597.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. C. Liu, S. Tzonev, S. Rebrik, and K. D. Miller
Variability and Information in a Neural Code of the Cat Lateral Geniculate Nucleus
J Neurophysiol,
December 1, 2001;
86(6):
2789 - 2806.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. W. Oram, N. G. Hatsopoulos, B. J. Richmond, and J. P. Donoghue
Excess Synchrony in Motor Cortical Neurons Provides Redundant Direction Information With That From Coarse Temporal Measures
J Neurophysiol,
October 1, 2001;
86(4):
1700 - 1716.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. R. Muller, A. B. Metha, J. Krauskopf, and P. Lennie
Information Conveyed by Onset Transients in Responses of Striate Cortical Neurons
J. Neurosci.,
September 1, 2001;
21(17):
6978 - 6990.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. E. Kass and V. Ventura
A Spike-Train Probability Model
Neural Comput.,
August 1, 2001;
13(8):
1713 - 1720.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. J. Chacron, A. Longtin, and L. Maler
Negative Interspike Interval Correlations Increase the Neuronal Capacity for Encoding Time-Dependent Stimuli
J. Neurosci.,
July 15, 2001;
21(14):
5328 - 5343.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Van Rullen and S. J. Thorpe
Rate Coding Versus Temporal Order Coding: What the Retinal Ganglion Cells Tell the Visual Cortex
Neural Comput.,
June 1, 2001;
13(6):
1255 - 1283.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Panzeri and S. R. Schultz
A Unified Approach to the Study of Temporal, Correlational, and Rate Coding
Neural Comput.,
June 1, 2001;
13(6):
1311 - 1349.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
V. Balasubramanian, D. Kimber, and M. J. Berry II
Metabolically Efficient Information Processing
Neural Comput.,
April 1, 2001;
13(4):
799 - 815.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
D. S. Reich, F. Mechler, and J. D. Victor
Formal and Attribute-Specific Information in Primary Visual Cortex
J Neurophysiol,
January 1, 2001;
85(1):
305 - 318.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A.-K. Warzecha, J. Kretzberg, and M. Egelhaaf
Reliability of a Fly Motion-Sensitive Neuron Depends on Stimulus Parameters
J. Neurosci.,
December 1, 2000;
20(23):
8886 - 8896.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Reinagel and R. C. Reid
Temporal Coding of Visual Information in the Thalamus
J. Neurosci.,
July 15, 2000;
20(14):
5392 - 5400.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Kreiman, R. Krahe, W. Metzner, C. Koch, and F. Gabbiani
Robustness and Variability of Neuronal Coding by Amplitude-Sensitive Afferents in the Weakly Electric Fish Eigenmannia
J Neurophysiol,
July 1, 2000;
84(1):
189 - 204.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Q. Pauluis and S. N. Baker
An Accurate Measure of the Instantaneous Discharge Probability, with Application to Unitary Joint-Event Analysis
Neural Comput.,
March 1, 2000;
12(3):
647 - 669.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
D. J. Mar, C. C. Chow, W. Gerstner, R. W. Adams, and J. J. Collins
Noise shaping in populations of coupled model neurons
PNAS,
August 31, 1999;
96(18):
10450 - 10455.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Kara and M. J. Friedlander
Arginine Analogs Modify Signal Detection by Neurons in the Visual Cortex
J. Neurosci.,
July 1, 1999;
19(13):
5528 - 5548.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. W. Oram, M. C. Wiener, R. Lestienne, and B. J. Richmond
Stochastic Nature of Precisely Timed Spike Patterns in Visual System Neuronal Responses
J Neurophysiol,
June 1, 1999;
81(6):
3021 - 3033.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Warzecha and M. Egelhaaf
Variability in Spike Trains During Constant and Dynamic Stimulation
Science,
March 19, 1999;
283(5409):
1927 - 1930.
[Abstract]
[Full Text]
| |