|
|
||||||||
The Journal of Neurophysiology Vol. 84 No. 3 September 2000, pp. 1488-1496
Copyright ©2000 by the American Physiological Society
1Department of Physiology and 2Department of Physics, Laval University, Quebec G1K 7P4, Canada; and 3Unité de Neurosciences Intégratives et Computatìonnelles, UPR 2191, Centre National de la Recherche Scientifique, 91198 Gif-sur-Yvette, France
Hô, Nicolas and
Alain Destexhe.
Synaptic Background Activity Enhances the Responsiveness of
Neocortical Pyramidal Neurons. J. Neurophysiol. 84: 1488-1496, 2000. Neocortical pyramidal neurons in vivo are
subject to an intense synaptic background activity but little is known
of how this activity affects cellular responsiveness and what function
it may serve. These issues were examined in morphologically
reconstructed neocortical pyramidal neurons in which synaptic
background activity was simulated based on recent measurements in cat
parietal cortex. We show that background activity can be decomposed
into two components: a tonically active conductance and voltage
fluctuations. Previous studies have mostly focused on the conductance
effect, revealing that background activity is responsible for a
decrease in responsiveness, which imposes severe conditions of
coincidence of inputs necessary to discharge the cell. It is shown
here, in contrast, that responsiveness is enhanced if voltage
fluctuations are taken into account; in this case the model can produce
responses to inputs that would normally be subthreshold. This effect is
analyzed by dissecting and comparing the different components of
background activity, as well as by evaluating the contribution of
parameters such as the dendritic morphology, the distribution of leak
currents, the value of axial resistivity, the densities of
voltage-dependent currents, and the release parameters underlying
background activity. Interestingly, the model's optimal responsiveness
was obtained when voltage fluctuations were of the same order as those
measured intracellularly in vivo. Possible consequences were also
investigated at the population level, where the presence of background
activity allowed networks of pyramidal neurons to instantaneously
detect inputs that are small compared with the classical detection
threshold. These results suggest, at the single-cell level, that the
presence of voltage fluctuations has a determining influence on
cellular responsiveness and that these should be taken into account in models of background activity. At the network level, we predict that
background activity provides the necessary drive for detecting events
that would normally be undetectable. Experiments are suggested to
explore this possible functional role for background activity.
This article has been cited by other articles:
![]() |
J. R. Binder, R. H. Desai, W. W. Graves, and L. L. Conant Where Is the Semantic System? A Critical Review and Meta-Analysis of 120 Functional Neuroimaging Studies Cereb Cortex, December 1, 2009; 19(12): 2767 - 2796. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Mirpour and H. Esteky State-Dependent Effects of Stimulus Presentation Duration on the Temporal Dynamics of Neural Responses in the Inferotemporal Cortex of Macaque Monkeys J Neurophysiol, September 1, 2009; 102(3): 1790 - 1800. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Hartwich, T. Pollak, and T. Klausberger Distinct Firing Patterns of Identified Basket and Dendrite-Targeting Interneurons in the Prefrontal Cortex during Hippocampal Theta and Local Spindle Oscillations J. Neurosci., July 29, 2009; 29(30): 9563 - 9574. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Nadim, V. Brezina, A. Destexhe, and C. Linster State Dependence of Network Output: Modeling and Experiments J. Neurosci., November 12, 2008; 28(46): 11806 - 11813. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Morita Possible Role of Dendritic Compartmentalization in the Spatial Working Memory Circuit J. Neurosci., July 23, 2008; 28(30): 7699 - 7724. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. P. Cook, J. A. Guest, Y. Liang, N. Y. Masse, and C. M. Colbert Dendrite-to-Soma Input/Output Function of Continuous Time-Varying Signals in Hippocampal CA1 Pyramidal Neurons J Neurophysiol, November 1, 2007; 98(5): 2943 - 2955. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Haider, A. Duque, A. R. Hasenstaub, Y. Yu, and D. A. McCormick Enhancement of Visual Responsiveness by Spontaneous Local Network Activity In Vivo J Neurophysiol, June 1, 2007; 97(6): 4186 - 4202. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Arsiero, H.-R. Luscher, B. N. Lundstrom, and M. Giugliano The Impact of Input Fluctuations on the Frequency-Current Relationships of Layer 5 Pyramidal Neurons in the Rat Medial Prefrontal Cortex J. Neurosci., March 21, 2007; 27(12): 3274 - 3284. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. S. Chance Receiver Operating Characteristic (ROC) Analysis for Characterizing Synaptic Efficacy J Neurophysiol, February 1, 2007; 97(2): 1799 - 1808. [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] |
||||
![]() |
A. Destexhe and D. Contreras Neuronal computations with stochastic network states. Science, October 6, 2006; 314(5796): 85 - 90. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. D. Micheva, C. P. Taylor, and S. J Smith Pregabalin Reduces the Release of Synaptic Vesicles from Cultured Hippocampal Neurons Mol. Pharmacol., August 1, 2006; 70(2): 467 - 476. [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] |
||||
![]() |
I. van Welie, J. A. van Hooft, and W. J. Wadman Background Activity Regulates Excitability of Rat Hippocampal CA1 Pyramidal Neurons by Adaptation of a K+ Conductance J Neurophysiol, March 1, 2006; 95(3): 2007 - 2012. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. S. Desai and E. C. Walcott Synaptic bombardment modulates muscarinic effects in forelimb motor cortex. J. Neurosci., February 22, 2006; 26(8): 2215 - 2226. [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] |
||||
![]() |
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] |
||||
![]() |
M. Rudolph, J. G. Pelletier, D. Pare, and A. Destexhe Characterization of Synaptic Conductances and Integrative Properties During Electrically Induced EEG-Activated States in Neocortical Neurons In Vivo J Neurophysiol, October 1, 2005; 94(4): 2805 - 2821. [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] |
||||
![]() |
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] |
||||
![]() |
K. M. Jacobs and D. A. Prince Excitatory and Inhibitory Postsynaptic Currents in a Rat Model of Epileptogenic Microgyria J Neurophysiol, February 1, 2005; 93(2): 687 - 696. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. S. G. Jones and G. L. Woodhall Background synaptic activity in rat entorhinal cortical neurones: differential control of transmitter release by presynaptic receptors J. Physiol., January 1, 2005; 562(1): 107 - 120. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Gervasoni, S.-C. Lin, S. Ribeiro, E. S. Soares, J. Pantoja, and M. A. L. Nicolelis Global Forebrain Dynamics Predict Rat Behavioral States and Their Transitions J. Neurosci., December 8, 2004; 24(49): 11137 - 11147. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Linkenkaer-Hansen, V. V. Nikulin, S. Palva, R. J. Ilmoniemi, and J. M. Palva Prestimulus Oscillations Enhance Psychophysical Performance in Humans J. Neurosci., November 10, 2004; 24(45): 10186 - 10190. [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] |
||||
![]() |
A. Korngreen Noise in the Foreground. Focus on "A Method to Estimate Synaptic Conductances From Membrane Potential Fluctuations" J Neurophysiol, June 1, 2004; 91(6): 2400 - 2400. [Full Text] [PDF] |
||||
![]() |
M. Rudolph, Z. Piwkowska, M. Badoual, T. Bal, and A. Destexhe A Method to Estimate Synaptic Conductances From Membrane Potential Fluctuations J Neurophysiol, June 1, 2004; 91(6): 2884 - 2896. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. A. Grande, G. A. Kinney, G. L. Miracle, and W. J. Spain Dynamic Influences on Coincidence Detection in Neocortical Pyramidal Neurons J. Neurosci., February 25, 2004; 24(8): 1839 - 1851. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Shu, A. Hasenstaub, M. Badoual, T. Bal, and D. A. McCormick Barrages of Synaptic Activity Control the Gain and Sensitivity of Cortical Neurons J. Neurosci., November 12, 2003; 23(32): 10388 - 10401. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. K. Murphy and K. D. Miller Multiplicative Gain Changes Are Induced by Excitation or Inhibition Alone J. Neurosci., November 5, 2003; 23(31): 10040 - 10051. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. V. Bui, S. Cushing, D. Dewey, R. E. Fyffe, and P. K. Rose Comparison of the Morphological and Electrotonic Properties of Renshaw Cells, Ia Inhibitory Interneurons, and Motoneurons in the Cat J Neurophysiol, November 1, 2003; 90(5): 2900 - 2918. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. A. McCormick, Y. Shu, A. Hasenstaub, M. Sanchez-Vives, M. Badoual, and T. Bal Persistent Cortical Activity: Mechanisms of Generation and Effects on Neuronal Excitability Cereb Cortex, November 1, 2003; 13(11): 1219 - 1231. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. K. Seamans, L. Nogueira, and A. Lavin Synaptic Basis of Persistent Activity in Prefrontal Cortex In Vivo and in Organotypic Cultures Cereb Cortex, November 1, 2003; 13(11): 1242 - 1250. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. Ariav, A. Polsky, and J. Schiller Submillisecond Precision of the Input-Output Transformation Function Mediated by Fast Sodium Dendritic Spikes in Basal Dendrites of CA1 Pyramidal Neurons J. Neurosci., August 27, 2003; 23(21): 7750 - 7758. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Holmgren, T. Harkany, B. Svennenfors, and Y. Zilberter Pyramidal cell communication within local networks in layer 2/3 of rat neocortex J. Physiol., August 15, 2003; 551(1): 139 - 153. [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] |
||||
![]() |
Z. Yang, I. Seif, and M. Armstrong-James Adult Experience-dependent Plasticity of S1 Barrel Cortex in the Normal and Monoamine Oxidase-A Knockout (Tg8) Mouse Cereb Cortex, December 1, 2002; 12(12): 1269 - 1279. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Magistretti and A. Alonso Fine Gating Properties of Channels Responsible for Persistent Sodium Current Generation in Entorhinal Cortex Neurons J. Gen. Physiol., November 25, 2002; 120(6): 855 - 873. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. E. Lewis and L. Maler Dynamics of Electrosensory Feedback: Short-Term Plasticity and Inhibition in a Parallel Fiber Pathway J Neurophysiol, October 1, 2002; 88(4): 1695 - 1706. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. H. Shalinsky, J. Magistretti, L. Ma, and A. A. Alonso Muscarinic Activation of a Cation Current and Associated Current Noise in Entorhinal-Cortex Layer-II Neurons J Neurophysiol, September 1, 2002; 88(3): 1197 - 1211. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. C. W. van Rossum, G. G. Turrigiano, and S. B. Nelson Fast Propagation of Firing Rates through Layered Networks of Noisy Neurons J. Neurosci., March 1, 2002; 22(5): 1956 - 1966. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. D. Miller and T. W. Troyer Neural Noise Can Explain Expansive, Power-Law Nonlinearities in Neural Response Functions J Neurophysiol, February 1, 2002; 87(2): 653 - 659. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. Fuhrmann, I. Segev, H. Markram, and M. Tsodyks Coding of Temporal Information by Activity-Dependent Synapses J Neurophysiol, January 1, 2002; 87(1): 140 - 148. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. S. Anderson, I. Lampl, D. C. Gillespie, and D. Ferster The Contribution of Noise to Contrast Invariance of Orientation Tuning in Cat Visual Cortex Science, December 8, 2000; 290(5498): 1968 - 1972. [Abstract] [Full Text] |
||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |