 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, August 15, 2000, 20(16):6193-6209
Impact of Correlated Synaptic Input on Output Firing Rate and Variability in Simple Neuronal Models
Emilio Salinas1 and Terrence J. Sejnowski2 1 Computational Neurobiology Laboratory, Howard Hughes Medical Institute, The Salk Institute for Biological Studies, La Jolla, California 92037, and 2 Department of Biology, University of California at San Diego, La Jolla, California 92093
Cortical neurons are typically driven by thousands of synaptic inputs. The arrival of a spike from one input may or may not be correlated with the arrival of other spikes from different inputs. How does this interdependence alter the probability that the postsynaptic neuron will fire? We constructed a simple random walk model in which the membrane potential of a target neuron fluctuates stochastically, driven by excitatory and inhibitory spikes arriving at random times. An analytic expression was derived for the mean output firing rate as a function of the firing rates and pairwise correlations of the inputs. This stochastic model made three quantitative predictions. (1) Correlations between pairs of excitatory or inhibitory inputs increase the fluctuations in synaptic drive, whereas correlations between excitatory-inhibitory pairs decrease them. (2) When excitation and inhibition are fully balanced (the mean net synaptic drive is zero), firing is caused by the fluctuations only. (3) In the balanced case, firing is irregular. These theoretical predictions were in excellent agreement with simulations of an integrate-and-fire neuron that included multiple conductances and received hundreds of synaptic inputs. The results show that, in the balanced regime, weak correlations caused by signals shared among inputs may have a multiplicative effect on the input-output rate curve of a postsynaptic neuron, i.e. they may regulate its gain; in the unbalanced regime, correlations may increase firing probability mainly around threshold, when output rate is low; and in all cases correlations are expected to increase the variability of the output spike train.
Key words: random-walk; integrate-and-fire; computer simulation; spike synchrony; oscillations; cross-correlation; balanced inhibition; cerebral cortex
Copyright © 2000 Society for Neuroscience 0270-6474/00/20166193-17$05.00/0
This article has been cited by other articles:
T. Tetzlaff, S. Rotter, E. Stark, M. Abeles, A. Aertsen, and M. Diesmann
Dependence of Neuronal Correlations on Filter Characteristics and Marginal Spike Train Statistics
Neural Comput., September 1, 2008; 20(9): 2133 - 2184.
[Abstract] [Full Text] [PDF]
B. Kriener, T. Tetzlaff, A. Aertsen, M. Diesmann, and S. Rotter
Correlations and Population Dynamics in Cortical Networks
Neural Comput., September 1, 2008; 20(9): 2185 - 2226.
[Abstract] [Full Text] [PDF]
K. Sakamoto, H. Mushiake, N. Saito, K. Aihara, M. Yano, and J. Tanji
Discharge Synchrony during the Transition of Behavioral Goal Representations Encoded by Discharge Rates of Prefrontal Neurons
Cereb Cortex, September 1, 2008; 18(9): 2036 - 2045.
[Abstract] [Full Text] [PDF]
R. Moreno-Bote, A. Renart, and N. Parga
Theory of Input Spike Auto- and Cross-Correlations and Their Effect on the Response of Spiking Neurons
Neural Comput., July 1, 2008; 20(7): 1651 - 1705.
[Abstract] [Full Text] [PDF]
P. Fries, T. Womelsdorf, R. Oostenveld, and R. Desimone
The Effects of Visual Stimulation and Selective Visual Attention on Rhythmic Neuronal Synchronization in Macaque Area V4
J. Neurosci., April 30, 2008; 28(18): 4823 - 4835.
[Abstract] [Full Text] [PDF]
K. Miura, Y. Tsubo, M. Okada, and T. Fukai
Balanced Excitatory and Inhibitory Inputs to Cortical Neurons Decouple Firing Irregularity from Rate Modulations
J. Neurosci., December 12, 2007; 27(50): 13802 - 13812.
[Abstract] [Full Text] [PDF]
Y. Yanai, N. Adamit, R. Harel, Z. Israel, and Y. Prut
Connected Corticospinal Sites Show Enhanced Tuning Similarity at the Onset of Voluntary Action
J. Neurosci., November 7, 2007; 27(45): 12349 - 12357.
[Abstract] [Full Text] [PDF]
B. Tripp and C. Eliasmith
Neural Populations Can Induce Reliable Postsynaptic Currents without Observable Spike Rate Changes or Precise Spike Timing
Cereb Cortex, August 1, 2007; 17(8): 1830 - 1840.
[Abstract] [Full Text] [PDF]
J. F. Medina and S. G. Lisberger
Variation, Signal, and Noise in Cerebellar Sensory-Motor Processing for Smooth-Pursuit Eye Movements
J. Neurosci., June 20, 2007; 27(25): 6832 - 6842.
[Abstract] [Full Text] [PDF]
Y. Liu, L. I. Zhang, and H. W. Tao
Heterosynaptic Scaling of Developing GABAergic Synapses: Dependence on Glutamatergic Input and Developmental Stage
J. Neurosci., May 16, 2007; 27(20): 5301 - 5312.
[Abstract] [Full Text] [PDF]
D. Durstewitz and T. Gabriel
Dynamical Basis of Irregular Spiking in NMDA-Driven Prefrontal Cortex Neurons
Cereb Cortex, April 1, 2007; 17(4): 894 - 908.
[Abstract] [Full Text] [PDF]
M. Siegel, T. H. Donner, R. Oostenveld, P. Fries, and A. K. Engel
High-Frequency Activity in Human Visual Cortex Is Modulated by Visual Motion Strength
Cereb Cortex, March 1, 2007; 17(3): 732 - 741.
[Abstract] [Full Text] [PDF]
I. M. Andolina, H. E. Jones, W. Wang, and A. M. Sillito
Corticothalamic feedback enhances stimulus response precision in the visual system
PNAS, January 30, 2007; 104(5): 1685 - 1690.
[Abstract] [Full Text] [PDF]
R. W. Berg, A. Alaburda, and J. Hounsgaard
Balanced Inhibition and Excitation Drive Spike Activity in Spinal Half-Centers
Science, January 19, 2007; 315(5810): 390 - 393.
[Abstract] [Full Text] [PDF]
K. M. Rodgers, A. M. Benison, and D. S. Barth
Two-Dimensional Coincidence Detection in the Vibrissa/Barrel Field
J Neurophysiol, October 1, 2006; 96(4): 1981 - 1990.
[Abstract] [Full Text] [PDF]
D. M. Devilbiss, M. E. Page, and B. D. Waterhouse
Locus Ceruleus Regulates Sensory Encoding by Neurons and Networks in Waking Animals
J. Neurosci., September 27, 2006; 26(39): 9860 - 9872.
[Abstract] [Full Text] [PDF]
M. Zeitler, P. Fries, and S. Gielen
Assessing neuronal coherence with single-unit, multi-unit, and local field potentials.
Neural Comput., September 1, 2006; 18(9): 2256 - 2281.
[Abstract] [Full Text] [PDF]
A. P. Sripati and K. O. Johnson
Dynamic Gain Changes During Attentional Modulation
Neural Comput., August 1, 2006; 18(8): 1847 - 1867.
[Abstract] [Full Text] [PDF]
R. M. Davies, G. L. Gerstein, and S. N. Baker
Measurement of Time-Dependent Changes in the Irregularity of Neural Spiking
J Neurophysiol, August 1, 2006; 96(2): 906 - 918.
[Abstract] [Full Text] [PDF]
M. J. Chacron
Nonlinear Information Processing in a Model Sensory System
J Neurophysiol, May 1, 2006; 95(5): 2933 - 2946.
[Abstract] [Full Text] [PDF]
B. Haider, A. Duque, A. R. Hasenstaub, and D. A. McCormick
Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition.
J. Neurosci., April 26, 2006; 26(17): 4535 - 4545.
[Abstract] [Full Text] [PDF]
T. J. Sejnowski and O. Paulsen
Network Oscillations: Emerging Computational Principles
J. Neurosci., February 8, 2006; 26(6): 1673 - 1676.
[Full Text] [PDF]
A. Renart, R. Moreno-Bote, X.-J. Wang, and N. Parga
Mean-Driven and Fluctuation-Driven Persistent Activity in Recurrent Networks
Neural Comput., January 1, 2006; 19(1): 1 - 46.
[Abstract] [Full Text] [PDF]
J. H. Kotaleski, D. Plenz, and K. T. Blackwell
Using Potassium Currents to Solve Signal-to-Noise Problems in Inhibitory Feedforward Networks of the Striatum
J Neurophysiol, January 1, 2006; 95(1): 331 - 341.
[Abstract] [Full Text] [PDF]
P. H. E. Tiesinga
Stimulus Competition by Inhibitory Interference
Neural Comput., November 1, 2005; 17(11): 2421 - 2453.
[Abstract] [Full Text] [PDF]
W. H. Mehaffey, B. Doiron, L. Maler, and R. W. Turner
Deterministic Multiplicative Gain Control with Active Dendrites
J. Neurosci., October 26, 2005; 25(43): 9968 - 9977.
[Abstract] [Full Text] [PDF]
R. Azouz
Dynamic Spatiotemporal Synaptic Integration in Cortical Neurons: Neuronal Gain, Revisited
J Neurophysiol, October 1, 2005; 94(4): 2785 - 2796.
[Abstract] [Full Text] [PDF]
C. Boucsein, M. Nawrot, S. Rotter, A. Aertsen, and D. Heck
Controlling Synaptic Input Patterns In Vitro by Dynamic Photo Stimulation
J Neurophysiol, October 1, 2005; 94(4): 2948 - 2958.
[Abstract] [Full Text] [PDF]
J. de la Rocha and N. Parga
Short-Term Synaptic Depression Causes a Non-Monotonic Response to Correlated Stimuli
J. Neurosci., September 14, 2005; 25(37): 8416 - 8431.
[Abstract] [Full Text] [PDF]
A. Morrison, C. Mehring, T. Geisel, A. Aertsen, and M. Diesmann
Advancing the Boundaries of High-Connectivity Network Simulation with Distributed Computing
Neural Comput., August 1, 2005; 17(8): 1776 - 1801.
[Abstract] [Full Text] [PDF]
K. Morita, K. Tsumoto, and K. Aihara
Possible Effects of Depolarizing GABAA Conductance on the Neuronal Input-Output Relationship: A Modeling Study
J Neurophysiol, June 1, 2005; 93(6): 3504 - 3523.
[Abstract] [Full Text] [PDF]
N. P. Bichot, A. F. Rossi, and R. Desimone
Parallel and Serial Neural Mechanisms for Visual Search in Macaque Area V4
Science, April 22, 2005; 308(5721): 529 - 534.
[Abstract] [Full Text] [PDF]
S. Mikula and E. Niebur
Rate and Synchrony in Feedforward Networks of Coincidence Detectors: Analytical Solution
Neural Comput., April 1, 2005; 17(4): 881 - 902.
[Abstract] [Full Text] [PDF]
J.-M. Schoffelen, R. Oostenveld, and P. Fries
Neuronal Coherence as a Mechanism of Effective Corticospinal Interaction
Science, April 1, 2005; 308(5718): 111 - 113.
[Abstract] [Full Text] [PDF]
M. Tomita and J. J. Eggermont
Cross-Correlation and Joint Spectro-Temporal Receptive Field Properties in Auditory Cortex
J Neurophysiol, January 1, 2005; 93(1): 378 - 392.
[Abstract] [Full Text] [PDF]
A. Benucci, P. F.M.J. Verschure, and P. Konig
Two-State Membrane Potential Fluctuations Driven by Weak Pairwise Correlations
Neural Comput., November 1, 2004; 16(11): 2351 - 2378.
[Abstract] [Full Text] [PDF]
B. S. Jackson
Including Long-Range Dependence in Integrate-and-Fire Models of the High Interspike-Interval Variability of Cortical Neurons
Neural Comput., October 1, 2004; 16(10): 2125 - 2195.
[Abstract] [Full Text] [PDF]
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]
N. Masuda and K. Aihara
Self-Organizing Dual Coding Based on Spike-Time-Dependent Plasticity
Neural Comput., March 1, 2004; 16(3): 627 - 663.
[Abstract] [Full Text] [PDF]
P.H.E. Tiesinga and T.J. Sejnowski
Rapid Temporal Modulation of Synchrony by Competition in Cortical Interneuron Networks
Neural Comput., February 1, 2004; 16(2): 251 - 275.
[Abstract] [Full Text] [PDF]
M. Rudolph and A. Destexhe
Characterization of Subthreshold Voltage Fluctuations in Neuronal Membranes
Neural Comput., November 1, 2003; 15(11): 2577 - 2618.
[Abstract] [Full Text] [PDF]
Y. Prut and S. I. Perlmutter
Firing Properties of Spinal Interneurons during Voluntary Movement. I. State-Dependent Regularity of Firing
J. Neurosci., October 22, 2003; 23(29): 9600 - 9610.
[Abstract] [Full Text] [PDF]
B. B. Averbeck and D. Lee
Neural Noise and Movement-Related Codes in the Macaque Supplementary Motor Area
J. Neurosci., August 20, 2003; 23(20): 7630 - 7641.
[Abstract] [Full Text] [PDF]
D. Lee
Coherent Oscillations in Neuronal Activity of the Supplementary Motor Area during a Visuomotor Task
J. Neurosci., July 30, 2003; 23(17): 6798 - 6809.
[Abstract] [Full Text] [PDF]
E. Salinas
Background Synaptic Activity as a Switch Between Dynamical States in a Network
Neural Comput., July 1, 2003; 15(7): 1439 - 1475.
[Abstract] [Full Text] [PDF]
Y. Aviel, C. Mehring, M. Abeles, and D. Horn
On Embedding Synfire Chains in a Balanced Network
Neural Comput., June 1, 2003; 15(6): 1321 - 1340.
[Abstract] [Full Text] [PDF]
E. T. Rolls, L. Franco, N. C. Aggelopoulos, and S. Reece
An Information Theoretic Approach to the Contributions of the Firing Rates and the Correlations Between the Firing of Neurons
J Neurophysiol, May 1, 2003; 89(5): 2810 - 2822.
[Abstract] [Full Text] [PDF]
J. D. Dorn and D. L. Ringach
Estimating Membrane Voltage Correlations From Extracellular Spike Trains
J Neurophysiol, April 1, 2003; 89(4): 2271 - 2278.
[Abstract] [Full Text] [PDF]
V. Litvak, H. Sompolinsky, I. Segev, and M. Abeles
On the Transmission of Rate Code in Long Feedforward Networks with Excitatory-Inhibitory Balance
J. Neurosci., April 1, 2003; 23(7): 3006 - 3015.
[Abstract] [Full Text] [PDF]
S. Mikula and E. Niebur
The Effects of Input Rate and Synchrony on a Coincidence Detector: Analytical Solution
Neural Comput., March 1, 2003; 15(3): 539 - 547.
[Abstract] [Full Text] [PDF]
S. A. Prescott and Y. De Koninck
Gain control of firing rate by shunting inhibition: Roles of synaptic noise and dendritic saturation
PNAS, February 18, 2003; 100(4): 2076 - 2081.
[Abstract] [Full Text] [PDF]
A. Kuhn, A. Aertsen, and S. Rotter
Higher-Order Statistics of Input Ensembles and the Response of Simple Model Neurons
Neural Comput., January 1, 2003; 15(1): 67 - 101.
[Abstract] [Full Text] [PDF]
N. Fourcaud and N. Brunel
Dynamics of the Firing Probability of Noisy Integrate-and-Fire Neurons
Neural Comput., September 1, 2002; 14(9): 2057 - 2110.
[Abstract] [Full Text] [PDF]
E. Salinas and T. J. Sejnowski
Integrate-and-Fire Neurons Driven by Correlated Stochastic Input
Neural Comput., September 1, 2002; 14(9): 2111 - 2155.
[Abstract] [Full Text] [PDF]
M. E. Raichle and D. A. Gusnard
Appraising the brain's energy budget
PNAS, August 6, 2002; 99(16): 10237 - 10239.
[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]
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]
S. A. Roy and K. D. Alloway
Coincidence Detection or Temporal Integration? What the Neurons in Somatosensory Cortex Are Doing
J. Neurosci., April 1, 2001; 21(7): 2462 - 2473.
[Abstract] [Full Text] [PDF]
P. Fries, J. H. Reynolds, A. E. Rorie, and R. Desimone
Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention
Science, February 23, 2001; 291(5508): 1560 - 1563.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|