Cerebral Cortex, Vol. 10, No. 9, 910-923,
September 2000
© 2000 Oxford University Press
Synaptic Mechanisms and Network Dynamics Underlying Spatial Working Memory in a Cortical Network Model
Volen Center for Complex Systems, Brandeis University, Waltham, MA 02254 and , 2 Section of Neurobiology, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510, USA
Single-neuron recordings from behaving primates have established a link between working memory processes and information-specific neuronal persistent activity in the prefrontal cortex. Using a network model endowed with a columnar architecture and based on the physiological properties of cortical neurons and synapses, we have examined the synaptic mechanisms of selective persistent activity underlying spatial working memory in the prefrontal cortex. Our model reproduces the phenomenology of the oculomotor delayed-response experiment of Funahashi et al. (S. Funahashi, C.J. Bruce and P.S. Goldman-Rakic, Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 61:331–349, 1989). To observe stable spontaneous and persistent activity, we find that recurrent synaptic excitation should be primarily mediated by NMDA receptors, and that overall recurrent synaptic interactions should be dominated by inhibition. Isodirectional tuning of adjacent pyramidal cells and interneurons can be accounted for by a structured pyramid-to-interneuron connectivity. Robust memory storage against random drift of the tuned persistent activity and against distractors (intervening stimuli during the delay period) may be enhanced by neuromodulation of recurrent synapses. Experimentally testable predictions concerning the neural basis of working memory are discussed.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. Duque and D. A. McCormick Circuit-based Localization of Ferret Prefrontal Cortex Cereb Cortex, September 7, 2009; (2009) bhp164v1. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Johnston, J. F. X. DeSouza, and S. Everling Monkey Prefrontal Cortical Pyramidal and Putative Interneurons Exhibit Differential Patterns of Activity Between Prosaccade and Antisaccade Tasks J. Neurosci., April 29, 2009; 29(17): 5516 - 5524. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Edin, T. Klingberg, P. Johansson, F. McNab, J. Tegner, and A. Compte Mechanism for top-down control of working memory capacity PNAS, April 21, 2009; 106(16): 6802 - 6807. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. A. Lewis, R. Y. Cho, C. S. Carter, K. Eklund, S. Forster, M. A. Kelly, and D. Montrose Subunit-Selective Modulation of GABA Type A Receptor Neurotransmission and Cognition in Schizophrenia Am J Psychiatry, December 1, 2008; 165(12): 1585 - 1593. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Tsujimoto, A. Genovesio, and S. P. Wise Transient Neuronal Correlations Underlying Goal Selection and Maintenance in Prefrontal Cortex Cereb Cortex, December 1, 2008; 18(12): 2748 - 2761. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Wang, G. G. Stradtman III, X.-J. Wang, and W.-J. Gao A specialized NMDA receptor function in layer 5 recurrent microcircuitry of the adult rat prefrontal cortex PNAS, October 28, 2008; 105(43): 16791 - 16796. [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]
|
|
|
|
 |
|
 M. Maniadakis and P. Trahanias Hierarchical Co-evolution of Cooperating Agents Acting in the Brain-Arena Adaptive Behavior, August 1, 2008; 16(4): 221 - 245. [Abstract] [PDF]
|
|
|
|
|
|
I. Diester and A. Nieder Complementary Contributions of Prefrontal Neuron Classes in Abstract Numerical Categorization J. Neurosci., July 30, 2008; 28(31): 7737 - 7747. [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]
|
|
|
|
 |
|
 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]
|
|
|
|
|
|
M. Winograd, A. Destexhe, and M. V. Sanchez-Vives Hyperpolarization-activated graded persistent activity in the prefrontal cortex PNAS, May 20, 2008; 105(20): 7298 - 7303. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Inoue and B. W. Strowbridge Transient Activity Induces a Long-Lasting Increase in the Excitability of Olfactory Bulb Interneurons J Neurophysiol, January 1, 2008; 99(1): 187 - 199. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. D. Van Hooser Similarity and Diversity in Visual Cortex: Is There a Unifying Theory of Cortical Computation? Neuroscientist, December 1, 2007; 13(6): 639 - 656. [Abstract] [PDF]
|
|
|
|
 |
|
 B. A. Milojkovic, W.-L. Zhou, and S. D. Antic Voltage and calcium transients in basal dendrites of the rat prefrontal cortex J. Physiol., December 1, 2007; 585(2): 447 - 468. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. A. A. van der Meer, J. J. Knierim, D. Yoganarasimha, E. R. Wood, and M. C. W. van Rossum Anticipation in the Rodent Head Direction System Can Be Explained by an Interaction of Head Movements and Vestibular Firing Properties J Neurophysiol, October 1, 2007; 98(4): 1883 - 1897. [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]
|
|
|
|
|
|
Y.-D. Zhou, A. Ardestani, and J. M. Fuster Distributed and Associative Working Memory Cereb Cortex, September 1, 2007; 17(suppl_1): i77 - i87. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Ardid, X.-J. Wang, and A. Compte An Integrated Microcircuit Model of Attentional Processing in the Neocortex J. Neurosci., August 8, 2007; 27(32): 8486 - 8495. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Botvinick and T. Watanabe From Numerosity to Ordinal Rank: A Gain-Field Model of Serial Order Representation in Cortical Working Memory J. Neurosci., August 8, 2007; 27(32): 8636 - 8642. [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]
|
|
|
|
|
|
L. Chen, J. D. Bohanick, M. Nishihara, J. K. Seamans, and C. R. Yang Dopamine D1/5 Receptor-Mediated Long-Term Potentiation of Intrinsic Excitability in Rat Prefrontal Cortical Neurons: Ca2+-Dependent Intracellular Signaling J Neurophysiol, March 1, 2007; 97(3): 2448 - 2464. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. B. Averbeck and D. Lee Prefrontal Neural Correlates of Memory for Sequences J. Neurosci., February 28, 2007; 27(9): 2204 - 2211. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Zaksas and T. Pasternak Directional Signals in the Prefrontal Cortex and in Area MT during a Working Memory for Visual Motion Task. J. Neurosci., November 8, 2006; 26(45): 11726 - 11742. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Cisek Integrated neural processes for defining potential actions and deciding between them: a computational model. J. Neurosci., September 20, 2006; 26(38): 9761 - 9770. [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]
|
|
|
|
 |
|
 K. Takehara-Nishiuchi, S. Kawahara, and Y. Kirino NMDA receptor-dependent processes in the medial prefrontal cortex are important for acquisition and the early stage of consolidation during trace, but not delay eyeblink conditioning Learn. Mem., November 1, 2005; 12(6): 606 - 614. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Lavin, L. Nogueira, C. C. Lapish, R. M. Wightman, P. E. M. Phillips, and J. K. Seamans Mesocortical Dopamine Neurons Operate in Distinct Temporal Domains Using Multimodal Signaling J. Neurosci., May 18, 2005; 25(20): 5013 - 5023. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Bandyopadhyay, C. Gonzalez-Islas, and J. J. Hablitz Dopamine Enhances Spatiotemporal Spread of Activity in Rat Prefrontal Cortex J Neurophysiol, February 1, 2005; 93(2): 864 - 872. [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]
|
|
|
|
|
|
C. Constantinidis and X.-J. Wang A Neural Circuit Basis for Spatial Working Memory Neuroscientist, December 1, 2004; 10(6): 553 - 565. [Abstract] [PDF]
|
|
|
|
|
|
F. Ostendorf, C. Finke, and C. J. Ploner Inhibition of Visual Discrimination During a Memory-Guided Saccade Task J Neurophysiol, July 1, 2004; 92(1): 660 - 664. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. A. Milojkovic, M. S. Radojicic, t. l. P. S. Goldman-Rakic, and S. D. Antic Burst generation in rat pyramidal neurones by regenerative potentials elicited in a restricted part of the basilar dendritic tree J. Physiol., July 1, 2004; 558(1): 193 - 211. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Winterer, R. Coppola, T. E. Goldberg, M. F. Egan, D. W. Jones, C. E. Sanchez, and D. R. Weinberger Prefrontal Broadband Noise, Working Memory, and Genetic Risk for Schizophrenia Am J Psychiatry, March 1, 2004; 161(3): 490 - 500. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
X.-J. Wang, J. Tegner, C. Constantinidis, and P. S. Goldman-Rakic Division of labor among distinct subtypes of inhibitory neurons in a cortical microcircuit of working memory PNAS, February 3, 2004; 101(5): 1368 - 1373. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. F. Glabus, B. Horwitz, J. L. Holt, P. D. Kohn, B. K. Gerton, J. H. Callicott, A. Meyer-Lindenberg, and K. F. Berman Interindividual Differences in Functional Interactions among Prefrontal, Parietal and Parahippocampal Regions during Working Memory Cereb Cortex, December 1, 2003; 13(12): 1352 - 1361. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R Vergara, C Rick, S Hernandez-Lopez, J A Laville, J N Guzman, E Galarraga, D J Surmeier, and J Bargas Spontaneous voltage oscillations in striatal projection neurons in a rat corticostriatal slice J. Physiol., November 15, 2003; 553(1): 169 - 182. [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]
|
|
|
|
|
|
G. N. Elston Cortex, Cognition and the Cell: New Insights into the Pyramidal Neuron and Prefrontal Function Cereb Cortex, November 1, 2003; 13(11): 1124 - 1138. [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]
|
|
|
|
|
|
C. D. Brody, A. Hernandez, A. Zainos, and R. Romo Timing and Neural Encoding of Somatosensory Parametric Working Memory in Macaque Prefrontal Cortex Cereb Cortex, November 1, 2003; 13(11): 1196 - 1207. [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]
|
|
|
|
|
|
T. Pasternak and D. Zaksas Stimulus Specificity and Temporal Dynamics of Working Memory for Visual Motion J Neurophysiol, October 1, 2003; 90(4): 2757 - 2762. [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]
|
|
|
|
 |
|
 C. B. Willmore The Cognitive Effect Profiles of NMDA Receptor Modulating Drugs are Resolvable If Stimulus Complexity Is Varied in a Number Discernment Task Behav Cogn Neurosci Rev, June 1, 2003; 2(2): 130 - 147. [Abstract] [PDF]
|
|
|
|
 |
|
 C. Pierrot-Deseilligny, R. M. Muri, C. J. Ploner, B. Gaymard, S. Demeret, and S. Rivaud-Pechoux Decisional role of the dorsolateral prefrontal cortex in ocular motor behaviour Brain, June 1, 2003; 126(6): 1460 - 1473. [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]
|
|
|
|
|
|
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]
|
|
|
|
|
|
C. Constantinidis and P. S. Goldman-Rakic Correlated Discharges Among Putative Pyramidal Neurons and Interneurons in the Primate Prefrontal Cortex J Neurophysiol, December 1, 2002; 88(6): 3487 - 3497. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Maccaferri and R. Dingledine Control of Feedforward Dendritic Inhibition by NMDA Receptor-Dependent Spike Timing in Hippocampal Interneurons J. Neurosci., July 1, 2002; 22(13): 5462 - 5472. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Degenetais, A.-M. Thierry, J. Glowinski, and Y. Gioanni Electrophysiological Properties of Pyramidal Neurons in the Rat Prefrontal Cortex: An In Vivo Intracellular Recording Study Cereb Cortex, January 1, 2002; 12(1): 1 - 16. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Gonzalez-Burgos and G. Barrionuevo Voltage-Gated Sodium Channels Shape Subthreshold EPSPs in Layer 5 Pyramidal Neurons From Rat Prefrontal Cortex J Neurophysiol, October 1, 2001; 86(4): 1671 - 1684. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Constantinidis, M. N. Franowicz, and P. S. Goldman-Rakic Coding Specificity in Cortical Microcircuits: A Multiple-Electrode Analysis of Primate Prefrontal Cortex J. Neurosci., May 15, 2001; 21(10): 3646 - 3655. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W.-J. Gao, L. S. Krimer, and P. S. Goldman-Rakic Presynaptic regulation of recurrent excitation by D1 receptors in prefrontal circuits PNAS, December 22, 2000; (2000) 11524298. [Abstract] [Full Text]
|
|
|
|
|
|
W.-J. Gao, L. S. Krimer, and P. S. Goldman-Rakic Presynaptic regulation of recurrent excitation by D1 receptors in prefrontal circuits PNAS, January 2, 2001; 98(1): 295 - 300. [Abstract] [Full Text] [PDF]
|
|