Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

Science 319 (5869): 1543-1546

Copyright © 2008 by the American Association for the Advancement of Science

Synaptic Theory of Working Memory

Gianluigi Mongillo,1*{dagger} Omri Barak,2* Misha Tsodyks2{ddagger}§

Abstract: It is usually assumed that enhanced spiking activity in the form of persistent reverberation for several seconds is the neural correlate of working memory. Here, we propose that working memory is sustained by calcium-mediated synaptic facilitation in the recurrent connections of neocortical networks. In this account, the presynaptic residual calcium is used as a buffer that is loaded, refreshed, and read out by spiking activity. Because of the long time constants of calcium kinetics, the refresh rate can be low, resulting in a mechanism that is metabolically efficient and robust. The duration and stability of working memory can be regulated by modulating the spontaneous activity in the network.

1 Group for Neural Theory, Département d'Etudes Cognitives, Ecole Normale Supérieure et Collège-de-France, Paris, France.
2 Department of Neurobiology, Weizmann Institute of Science, Rehovot, Israel.

* These authors contributed equally to this work.

{dagger} Present address: Laboratoire de Neurophysique et Physiologie, Université Paris-Descartes, CNRS-UMR8119, and Franco-Israeli Laboratory of System Neurophysiology and Neurophysics, Paris, France.

{ddagger} CNRS visiting member of the Group for Neural Theory, Ecole Normale Supérieure et Collège-de-France.

§ To whom correspondence should be addressed. E-mail: misha{at}weizmann.ac.il


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
The Cell-Type Specific Cortical Microcircuit: Relating Structure and Activity in a Full-Scale Spiking Network Model.
T. C. Potjans and M. Diesmann (2014)
Cereb Cortex 24, 785-806
   Abstract »    Full Text »    PDF »
Correspondence Between Stimulus Encoding- and Maintenance-Related Neural Processes Underlies Successful Working Memory.
J. R. Cohen, K. K. Sreenivasan, and M. D'Esposito (2014)
Cereb Cortex 24, 593-599
   Abstract »    Full Text »    PDF »
Causal Evidence for a Privileged Working Memory State in Early Visual Cortex.
N. Zokaei, S. Manohar, M. Husain, and E. Feredoes (2014)
J. Neurosci. 34, 158-162
   Abstract »    Full Text »    PDF »
Short-term synaptic plasticity in the deterministic Tsodyks-Markram model leads to unpredictable network dynamics.
J. M. Cortes, M. Desroches, S. Rodrigues, R. Veltz, M. A. Munoz, and T. J. Sejnowski (2013)
PNAS 110, 16610-16615
   Abstract »    Full Text »    PDF »
Synaptic Mechanisms Underlying Strong Reciprocal Connectivity between the Medial Prefrontal Cortex and Basolateral Amygdala.
J. P. Little and A. G. Carter (2013)
J. Neurosci. 33, 15333-15342
   Abstract »    Full Text »    PDF »
Selective visual processing across competition episodes: a theory of task-driven visual attention and working memory.
W. X. Schneider (2013)
Phil Trans R Soc B 368, 20130060
   Abstract »    Full Text »    PDF »
Theta Oscillations in the Medial Prefrontal Cortex Are Modulated by Spatial Working Memory and Synchronize with the Hippocampus through Its Ventral Subregion.
P.-K. O'Neill, J. A. Gordon, and T. Sigurdsson (2013)
J. Neurosci. 33, 14211-14224
   Abstract »    Full Text »    PDF »
Control of layer 5 pyramidal cell spiking by oscillatory inhibition in the distal apical dendrites: a computational modeling study.
X. Li, K. Morita, H. P. C. Robinson, and M. Small (2013)
J Neurophysiol 109, 2739-2756
   Abstract »    Full Text »    PDF »
Quantitative examination of stimulus-response relations in cortical networks in vitro.
O. Weihberger, S. Okujeni, J. E. Mikkonen, and U. Egert (2013)
J Neurophysiol 109, 1764-1774
   Abstract »    Full Text »    PDF »
Short-Term Memory in Networks of Dissociated Cortical Neurons.
M. R. Dranias, H. Ju, E. Rajaram, and A. M. J. VanDongen (2013)
J. Neurosci. 33, 1940-1953
   Abstract »    Full Text »    PDF »
Common Rules Guide Comparisons of Speed and Direction of Motion in the Dorsolateral Prefrontal Cortex.
C. R. Hussar and T. Pasternak (2013)
J. Neurosci. 33, 972-986
   Abstract »    Full Text »    PDF »
Short-Term Plasticity Explains Irregular Persistent Activity in Working Memory Tasks.
D. Hansel and G. Mato (2013)
J. Neurosci. 33, 133-149
   Abstract »    Full Text »    PDF »
Task-Relevant and Accessory Items in Working Memory Have Opposite Effects on Activity in Extrastriate Cortex.
J. C. Peters, P. R. Roelfsema, and R. Goebel (2012)
J. Neurosci. 32, 17003-17011
   Abstract »    Full Text »    PDF »
Nonconserved Ca2+/Calmodulin Binding Sites in Munc13s Differentially Control Synaptic Short-Term Plasticity.
N. Lipstein, S. Schaks, K. Dimova, S. Kalkhof, C. Ihling, K. Kolbel, U. Ashery, J. Rhee, N. Brose, A. Sinz, et al. (2012)
Mol. Cell. Biol. 32, 4628-4641
   Abstract »    Full Text »    PDF »
Fundamental limits on persistent activity in networks of noisy neurons.
Y. Burak and I. R. Fiete (2012)
PNAS 109, 17645-17650
   Abstract »    Full Text »    PDF »
Dynamic afferent synapses to decision-making networks improve performance in tasks requiring stimulus associations and discriminations.
M. A. Bourjaily and P. Miller (2012)
J Neurophysiol 108, 513-527
   Abstract »    Full Text »    PDF »
Hyperconnectivity and Slow Synapses during Early Development of Medial Prefrontal Cortex in a Mouse Model for Mental Retardation and Autism.
G. Testa-Silva, A. Loebel, M. Giugliano, C. P. J. de Kock, H. D. Mansvelder, and R. M. Meredith (2012)
Cereb Cortex 22, 1333-1342
   Abstract »    Full Text »    PDF »
Altered axonal targeting and short-term plasticity in the hippocampus of Disc1 mutant mice.
M. Kvajo, H. McKellar, L. J. Drew, A.-M. Lepagnol-Bestel, L. Xiao, R. J. Levy, R. Blazeski, P. A. Arguello, C. O. Lacefield, C. A. Mason, et al. (2011)
PNAS 108, E1349-E1358
   Abstract »    Full Text »    PDF »
Representation of comparison signals in cortical area MT during a delayed direction discrimination task.
L. L. Lui and T. Pasternak (2011)
J Neurophysiol 106, 1260-1273
   Abstract »    Full Text »    PDF »
Abnormal Presynaptic Short-Term Plasticity and Information Processing in a Mouse Model of Fragile X Syndrome.
P.-Y. Deng, D. Sojka, and V. A. Klyachko (2011)
J. Neurosci. 31, 10971-10982
   Abstract »    Full Text »    PDF »
Highly Differentiated Projection-Specific Cortical Subnetworks.
M. Morishima, K. Morita, Y. Kubota, and Y. Kawaguchi (2011)
J. Neurosci. 31, 10380-10391
   Abstract »    Full Text »    PDF »
Neural and computational mechanisms of postponed decisions.
M. Martinez-Garcia, E. T. Rolls, G. Deco, and R. Romo (2011)
PNAS 108, 11626-11631
   Abstract »    Full Text »    PDF »
Post-tetanic increase in the fast-releasing synaptic vesicle pool at the expense of the slowly releasing pool.
J. S. Lee, W.-K. Ho, and S.-H. Lee (2010)
J. Gen. Physiol. 136, 259-272
   Abstract »    Full Text »    PDF »
Beneficial Effects of the NMDA Antagonist Ketamine on Decision Processes in Visual Search.
K. Shen, S. Kalwarowsky, W. Clarence, E. Brunamonti, and M. Pare (2010)
J. Neurosci. 30, 9947-9953
   Abstract »    Full Text »    PDF »
Neuronal Population Coding of Parametric Working Memory.
O. Barak, M. Tsodyks, and R. Romo (2010)
J. Neurosci. 30, 9424-9430
   Abstract »    Full Text »    PDF »
Hierarchical Interaction Structure of Neural Activities in Cortical Slice Cultures.
G. S. Santos, E. D. Gireesh, D. Plenz, and H. Nakahara (2010)
J. Neurosci. 30, 8720-8733
   Abstract »    Full Text »    PDF »
Temporal delays among place cells determine the frequency of population theta oscillations in the hippocampus.
C. Geisler, K. Diba, E. Pastalkova, K. Mizuseki, S. Royer, and G. Buzsaki (2010)
PNAS 107, 7957-7962
   Abstract »    Full Text »    PDF »
Synaptic dynamics and decision making.
G. Deco, E. T. Rolls, and R. Romo (2010)
PNAS 107, 7545-7549
   Abstract »    Full Text »    PDF »
Stimulation of the Frontal Eye Field Reveals Persistent Effective Connectivity after Controlled Behavior.
R. Akaishi, Y. Morishima, V. P. Rajeswaren, S. Aoki, and K. Sakai (2010)
J. Neurosci. 30, 4295-4305
   Abstract »    Full Text »    PDF »
Mechanisms underlying short-term modulation of transmitter release by presynaptic depolarization.
T. Hori and T. Takahashi (2009)
J. Physiol. 587, 2987-3000
   Abstract »    Full Text »    PDF »
Neural Dynamics in Inferior Temporal Cortex during a Visual Working Memory Task.
L. Woloszyn and D. L. Sheinberg (2009)
J. Neurosci. 29, 5494-5507
   Abstract »    Full Text »    PDF »
Homeostatic Presynaptic Suppression of Neuronal Network Bursts.
D. Cohen and M. Segal (2009)
J Neurophysiol 101, 2077-2088
   Abstract »    Full Text »    PDF »
Intermittent ambiguous stimuli: Implicit memory causes periodic perceptual alternations.
J. W. Brascamp, J. Pearson, R. Blake, and A. V. van den Berg (2009)
J Vis 9, 3
   Abstract »    Full Text »    PDF »
Broadband Coding with Dynamic Synapses.
B. Lindner, D. Gangloff, A. Longtin, and J. E. Lewis (2009)
J. Neurosci. 29, 2076-2087
   Abstract »    Full Text »    PDF »
Interaction of Cellular and Network Mechanisms in Spatiotemporal Pattern Formation in Neuronal Networks.
A. Bogaard, J. Parent, M. Zochowski, and V. Booth (2009)
J. Neurosci. 29, 1677-1687
   Abstract »    Full Text »    PDF »
State-, Timing-, and Pattern-Dependent Neuromodulation of Synaptic Strength by a Serotonergic Interneuron.
A. Sakurai and P. S. Katz (2009)
J. Neurosci. 29, 268-279
   Abstract »    Full Text »    PDF »
Memory traces in dynamical systems.
S. Ganguli, D. Huh, and H. Sompolinsky (2008)
PNAS 105, 18970-18975
   Abstract »    Full Text »    PDF »
A specialized NMDA receptor function in layer 5 recurrent microcircuitry of the adult rat prefrontal cortex.
H. Wang, G. G. Stradtman III, X.-J. Wang, and W.-J. Gao (2008)
PNAS 105, 16791-16796
   Abstract »    Full Text »    PDF »
Temporary Activation of Long-Term Memory Supports Working Memory.
J. A. Lewis-Peacock and B. R. Postle (2008)
J. Neurosci. 28, 8765-8771
   Abstract »    Full Text »    PDF »
NEUROSCIENCE: A Quiescent Working Memory.
S. Fusi (2008)
Science 319, 1495-1496
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882