 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, November 1, 1999, 19(21):9587-9603
Synaptic Basis of Cortical Persistent Activity: the Importance of NMDA Receptors to Working Memory
Xiao-Jing Wang Volen Center for Complex Systems and Department of Physics, Brandeis University, Waltham, Massachusetts 02454-9110
Delay-period activity of prefrontal cortical cells, the neural hallmark of working memory, is generally assumed to be sustained by reverberating synaptic excitation in the prefrontal cortical circuit. Previous model studies of working memory emphasized the high efficacy of recurrent synapses, but did not investigate the role of temporal synaptic dynamics. In this theoretical work, I show that biophysical properties of cortical synaptic transmission are important to the generation and stabilization of a network persistent state. This is especially the case when negative feedback mechanisms (such as spike-frequency adaptation, feedback shunting inhibition, and short-term depression of recurrent excitatory synapses) are included so that the neural firing rates are controlled within a physiological range (10-50 Hz), in spite of the exuberant recurrent excitation. Moreover, it is found that, to achieve a stable persistent state, recurrent excitatory synapses must be dominated by a slow component. If neuronal firings are asynchronous, the synaptic decay time constant needs to be comparable to that of the negative feedback; whereas in the case of partially synchronous dynamics, it needs to be comparable to a typical interspike interval (or oscillation period). Slow synaptic current kinetics also leads to the saturation of synaptic drive at high firing frequencies that contributes to rate control in a persistent state. For these reasons the slow NMDA receptor-mediated synaptic transmission is likely required for sustaining persistent network activity at low firing rates. This result suggests a critical role of the NMDA receptor channels in normal working memory function of the prefrontal cortex.
Key words: working memory; prefrontal cortex; persistent activity; NMDA receptor; synaptic dynamics; short-term plasticity; rate control; synchronization; spiking neuron model
Copyright © 1999 Society for Neuroscience 0270-6474/99/19219587-17$05.00/0
This article has been cited by other articles:
M. Nikitchenko and A. Koulakov
Neural Integrator: A Sandpile Model
Neural Comput., October 1, 2008; 20(10): 2379 - 2417.
[Abstract] [Full Text] [PDF]
S. Romani, D. J. Amit, and Y. Amit
Optimizing One-Shot Learning with Binary Synapses
Neural Comput., August 1, 2008; 20(8): 1928 - 1950.
[Abstract] [Full Text] [PDF]
K. Thurley, W. Senn, and H.-R. Luscher
Dopamine Increases the Gain of the Input-Output Response of Rat Prefrontal Pyramidal Neurons
J Neurophysiol, June 1, 2008; 99(6): 2985 - 2997.
[Abstract] [Full Text] [PDF]
C. I. Buia and P. H. Tiesinga
Role of Interneuron Diversity in the Cortical Microcircuit for Attention
J Neurophysiol, May 1, 2008; 99(5): 2158 - 2182.
[Abstract] [Full Text] [PDF]
N. Axmacher, D. P. Schmitz, I. Weinreich, C. E. Elger, and J. Fell
Interaction of Working Memory and Long-Term Memory in the Medial Temporal Lobe
Cereb Cortex, April 9, 2008; (2008) bhn045v1.
[Abstract] [Full Text] [PDF]
H. Trantham-Davidson, S. Kroner, and J. K. Seamans
Dopamine Modulation of Prefrontal Cortex Interneurons Occurs Independently of DARPP-32
Cereb Cortex, April 1, 2008; 18(4): 951 - 958.
[Abstract] [Full Text] [PDF]
C. K. Machens and C. D. Brody
Design of Continuous Attractor Networks with Monotonic Tuning Using a Symmetry Principle
Neural Comput., February 1, 2008; 20(2): 452 - 485.
[Abstract] [Full Text] [PDF]
J. P. Larsson, F. Vera Constan, N. Sebastian-Galles, and G. Deco
Lexical plasticity in early bilinguals does not alter phoneme categories: I. Neurodynamical modeling.
J. Cogn. Neurosci., January 1, 2008; 20(1): 76 - 94.
[Abstract] [Full Text] [PDF]
L. de Almeida, M. Idiart, and J. E. Lisman
Memory retrieval time and memory capacity of the CA3 network: Role of gamma frequency oscillations
Learn. Mem., November 15, 2007; 14(11): 795 - 806.
[Abstract] [Full Text] [PDF]
C. Bartolozzi and G. Indiveri
Synaptic Dynamics in Analog VLSI
Neural Comput., October 1, 2007; 19(10): 2581 - 2603.
[Abstract] [Full Text] [PDF]
R. Moreno-Bote, J. Rinzel, and N. Rubin
Noise-Induced Alternations in an Attractor Network Model of Perceptual Bistability
J Neurophysiol, September 1, 2007; 98(3): 1125 - 1139.
[Abstract] [Full Text] [PDF]
E. Carter and X.-J. Wang
Cannabinoid-Mediated Disinhibition and Working Memory: Dynamical Interplay of Multiple Feedback Mechanisms in a Continuous Attractor Model of Prefrontal Cortex
Cereb Cortex, September 1, 2007; 17(suppl_1): i16 - i26.
[Abstract] [Full Text] [PDF]
H.-Y. Tan, J. H. Callicott, and D. R. Weinberger
Dysfunctional and Compensatory Prefrontal Cortical Systems, Genes and the Pathogenesis of Schizophrenia
Cereb Cortex, September 1, 2007; 17(suppl_1): i171 - i181.
[Abstract] [Full Text] [PDF]
C. Ly and D. Tranchina
Critical analysis of dimension reduction by a moment closure method in a population density approach to neural network modeling.
Neural Comput., August 1, 2007; 19(8): 2032 - 2092.
[Abstract] [Full Text] [PDF]
H.-Y. Tan, Q. Chen, S. Sust, J. W. Buckholtz, J. D. Meyers, M. F. Egan, V. S. Mattay, A. Meyer-Lindenberg, D. R. Weinberger, and J. H. Callicott
Epistasis between catechol-O-methyltransferase and type II metabotropic glutamate receptor 3 genes on working memory brain function
PNAS, July 24, 2007; 104(30): 12536 - 12541.
[Abstract] [Full Text] [PDF]
A. Mouri, Y. Noda, A. Noda, T. Nakamura, T. Tokura, Y. Yura, A. Nitta, H. Furukawa, and T. Nabeshima
Involvement of a Dysfunctional Dopamine-D1/N-Methyl-D-aspartate-NR1 and Ca2+/Calmodulin-Dependent Protein Kinase II Pathway in the Impairment of Latent Learning in a Model of Schizophrenia Induced by Phencyclidine
Mol. Pharmacol., June 1, 2007; 71(6): 1598 - 1609.
[Abstract] [Full Text] [PDF]
Y. Tu, S. Kroener, K. Abernathy, C. Lapish, J. Seamans, L. J. Chandler, and J. J. Woodward
Ethanol Inhibits Persistent Activity in Prefrontal Cortical Neurons
J. Neurosci., April 25, 2007; 27(17): 4765 - 4775.
[Abstract] [Full Text] [PDF]
A. Kepecs and S. Raghavachari
Gating Information by Two-State Membrane Potential Fluctuations
J Neurophysiol, April 1, 2007; 97(4): 3015 - 3023.
[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]
F. C. Joelving, A. Compte, and C. Constantinidis
Temporal Properties of Posterior Parietal Neuron Discharges During Working Memory and Passive Viewing
J Neurophysiol, March 1, 2007; 97(3): 2254 - 2266.
[Abstract] [Full Text] [PDF]
G. La Camera, A. Rauch, D. Thurbon, H.-R. Luscher, W. Senn, and S. Fusi
Multiple Time Scales of Temporal Response in Pyramidal and Fast Spiking Cortical Neurons
J Neurophysiol, December 1, 2006; 96(6): 3448 - 3464.
[Abstract] [Full Text] [PDF]
R. C. O'Reilly
Biologically based computational models of high-level cognition.
Science, October 6, 2006; 314(5796): 91 - 94.
[Abstract] [Full Text] [PDF]
R. Singh and C. Eliasmith
Higher-dimensional neurons explain the tuning and dynamics of working memory cells.
J. Neurosci., April 5, 2006; 26(14): 3667 - 3678.
[Abstract] [Full Text] [PDF]
P. Miller and X.-J. Wang
Power-Law Neuronal Fluctuations in a Recurrent Network Model of Parametric Working Memory
J Neurophysiol, February 1, 2006; 95(2): 1099 - 1114.
[Abstract] [Full Text] [PDF]
D. Golomb, A. Shedmi, R. Curtu, and G. B. Ermentrout
Persistent Synchronized Bursting Activity in Cortical Tissues With Low Magnesium Concentration: A Modeling Study
J Neurophysiol, February 1, 2006; 95(2): 1049 - 1067.
[Abstract] [Full Text] [PDF]
K.-F. Wong and X.-J. Wang
A Recurrent Network Mechanism of Time Integration in Perceptual Decisions
J. Neurosci., January 25, 2006; 26(4): 1314 - 1328.
[Abstract] [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]
A. V. Rangan, D. Cai, and D. W. McLaughlin
Inaugural Article: Modeling the spatiotemporal cortical activity associated with the line-motion illusion in primary visual cortex
PNAS, December 27, 2005; 102(52): 18793 - 18800.
[Abstract] [Full Text] [PDF]
J. H. Krystal, E. B. Perry Jr, R. Gueorguieva, A. Belger, S. H. Madonick, A. Abi-Dargham, T. B. Cooper, L. MacDougall, W. Abi-Saab, and D. C. D'Souza
Comparative and Interactive Human Psychopharmacologic Effects of Ketamine and Amphetamine: Implications for Glutamatergic and Dopaminergic Model Psychoses and Cognitive Function
Arch Gen Psychiatry, September 1, 2005; 62(9): 985 - 994.
[Abstract] [Full Text] [PDF]
P.-M. Lau and G.-Q. Bi
Synaptic mechanisms of persistent reverberatory activity in neuronal networks
PNAS, July 19, 2005; 102(29): 10333 - 10338.
[Abstract] [Full Text] [PDF]
C. Wyart, S. Cocco, L. Bourdieu, J.-F. Leger, C. Herr, and D. Chatenay
Dynamics of Excitatory Synaptic Components in Sustained Firing at Low Rates
J Neurophysiol, June 1, 2005; 93(6): 3370 - 3380.
[Abstract] [Full Text] [PDF]
A. R. Houweling, M. Bazhenov, I. Timofeev, M. Steriade, and T. J. Sejnowski
Homeostatic Synaptic Plasticity Can Explain Post-traumatic Epileptogenesis in Chronically Isolated Neocortex
Cereb Cortex, June 1, 2005; 15(6): 834 - 845.
[Abstract] [Full Text] [PDF]
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]
Y. Aviel, D. Horn, and M. Abeles
Memory Capacity of Balanced Networks
Neural Comput., March 1, 2005; 17(3): 691 - 713.
[Abstract] [Full Text] [PDF]
P. Song and X.-J. Wang
Angular Path Integration by Moving "Hill of Activity": A Spiking Neuron Model without Recurrent Excitation of the Head-Direction System
J. Neurosci., January 26, 2005; 25(4): 1002 - 1014.
[Abstract] [Full Text] [PDF]
G. Deco and E. T. Rolls
Synaptic and Spiking Dynamics underlying Reward Reversal in the Orbitofrontal Cortex
Cereb Cortex, January 1, 2005; 15(1): 15 - 30.
[Abstract] [Full Text] [PDF]
C. Constantinidis and X.-J. Wang
A Neural Circuit Basis for Spatial Working Memory
Neuroscientist, December 1, 2004; 10(6): 553 - 565.
[Abstract] [PDF]
S. Fujisawa, N. Matsuki, and Y. Ikegaya
Chronometric readout from a memory trace: gamma-frequency field stimulation recruits timed recurrent activity in the rat CA3 network
J. Physiol., November 15, 2004; 561(1): 123 - 131.
[Abstract] [Full Text] [PDF]
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]
P. E. Latham and S. Nirenberg
Computing and Stability in Cortical Networks
Neural Comput., July 1, 2004; 16(7): 1385 - 1412.
[Abstract] [Full Text] [PDF]
L. M. de la Prida and B. Gal
Synaptic Contributions to Focal and Widespread Spatiotemporal Dynamics in the Isolated Rat Subiculum In Vitro
J. Neurosci., June 16, 2004; 24(24): 5525 - 5536.
[Abstract] [Full Text] [PDF]
G. Deco, E. T. Rolls, and B. Horwitz
"What" and "Where" in Visual Working Memory: A Computational Neurodynamical Perspective for Integrating fMRI and Single-Neuron Data
J. Cogn. Neurosci., May 1, 2004; 16(4): 683 - 701.
[Abstract] [Full Text] [PDF]
L. Tao, M. Shelley, D. McLaughlin, and R. Shapley
An egalitarian network model for the emergence of simple and complex cells in visual cortex
PNAS, January 6, 2004; 101(1): 366 - 371.
[Abstract] [Full Text] [PDF]
B. Ermentrout
Dynamical Consequences of Fast-Rising, Slow-Decaying Synapses in Neuronal Networks
Neural Comput., November 1, 2003; 15(11): 2483 - 2522.
[Abstract] [Full Text] [PDF]
A. Compte,, C. Constantinidis, J. Tegner, S. Raghavachari, M. V. Chafee, P. S. Goldman-Rakic, and X.-J. Wang
Temporally Irregular Mnemonic Persistent Activity in Prefrontal Neurons of Monkeys During a Delayed Response Task
J Neurophysiol, November 1, 2003; 90(5): 3441 - 3454.
[Abstract] [Full Text] [PDF]
D. J. Amit and G. Mongillo
Selective Delay Activity in the Cortex: Phenomena and Interpretation
Cereb Cortex, November 1, 2003; 13(11): 1139 - 1150.
[Abstract] [Full Text] [PDF]
N. Brunel
Dynamics and Plasticity of Stimulus-selective Persistent Activity in Cortical Network Models
Cereb Cortex, November 1, 2003; 13(11): 1151 - 1161.
[Abstract] [Full Text] [PDF]
P. Miller, C. D Brody, R. Romo, and X.-J. Wang
A Recurrent Network Model of Somatosensory Parametric Working Memory in the Prefrontal Cortex
Cereb Cortex, November 1, 2003; 13(11): 1208 - 1218.
[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]
C. I. O. Myme, K. Sugino, G. G. Turrigiano, and S. B. Nelson
The NMDA-to-AMPA Ratio at Synapses Onto Layer 2/3 Pyramidal Neurons Is Conserved Across Prefrontal and Visual Cortices
J Neurophysiol, August 1, 2003; 90(2): 771 - 779.
[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]
N. Brunel and X.-J. Wang
What Determines the Frequency of Fast Network Oscillations With Irregular Neural Discharges? I. Synaptic Dynamics and Excitation-Inhibition Balance
J Neurophysiol, July 1, 2003; 90(1): 415 - 430.
[Abstract] [Full Text] [PDF]
D.J. Amit, A. Bernacchia, and V. Yakovlev
Multiple-object Working Memory--A Model for Behavioral Performance
Cereb Cortex, May 1, 2003; 13(5): 435 - 443.
[Abstract] [Full Text] [PDF]
P. J. Drew and L. F. Abbott
Model of Song Selectivity and Sequence Generation in Area HVc of the Songbird
J Neurophysiol, May 1, 2003; 89(5): 2697 - 2706.
[Abstract] [Full Text] [PDF]
A. Compte, M. V. Sanchez-Vives, D. A. McCormick, and X.-J. Wang
Cellular and Network Mechanisms of Slow Oscillatory Activity (<1 Hz) and Wave Propagations in a Cortical Network Model
J Neurophysiol, May 1, 2003; 89(5): 2707 - 2725.
[Abstract] [Full Text] [PDF]
J. Reutimann, M. Giugliano, and S. Fusi
Event-Driven Simulation of Spiking Neurons with Stochastic Dynamics
Neural Comput., April 1, 2003; 15(4): 811 - 830.
[Abstract] [Full Text] [PDF]
K. Kang, M. Shelley, and H. Sompolinsky
Mexican hats and pinwheels in visual cortex
PNAS, March 4, 2003; 100(5): 2848 - 2853.
[Abstract] [Full Text] [PDF]
D. Hansel and G. Mato
Asynchronous States and the Emergence of Synchrony in Large Networks of Interacting Excitatory and Inhibitory Neurons
Neural Comput., January 1, 2003; 15(1): 1 - 56.
[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]
