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 304 (5670): 559-564

Copyright © 2004 by the American Association for the Advancement of Science

Synfire Chains and Cortical Songs: Temporal Modules of Cortical Activity

Yuji Ikegaya,1* Gloster Aaron,1* Rosa Cossart,1 Dmitriy Aronov,1 Ilan Lampl,2 David Ferster,2 Rafael Yuste1{dagger}

Abstract: How can neural activity propagate through cortical networks built with weak, stochastic synapses? We find precise repetitions of spontaneous patterns of synaptic inputs in neocortical neurons in vivo and in vitro. These patterns repeat after minutes, maintaining millisecond accuracy. Calcium imaging of slices reveals reactivation of sequences of cells during the occurrence of repeated intracellular synaptic patterns. The spontaneous activity drifts with time, engaging different cells. Sequences of active neurons have distinct spatial structures and are repeated in the same order over tens of seconds, revealing modular temporal dynamics. Higher order sequences are replayed with compressed timing.

1 Department of Biological Sciences, Columbia University, New York, NY 10027, USA.
2 Department of Neurobiology and Physiology, Northwestern University, Evanston, IL 60208, USA.

Back to Top

* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: rmy5{at}columbia.edu


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Timing as an intrinsic property of neural networks: evidence from in vivo and in vitro experiments.
A. Goel and D. V. Buonomano (2014)
Phil Trans R Soc B 369, 20120460
   Abstract »    Full Text »    PDF »
Laminar and Columnar Structure of Sensory-Evoked Multineuronal Spike Sequences in Adult Rat Barrel Cortex In Vivo.
V. Reyes-Puerta, J.-J. Sun, S. Kim, W. Kilb, and H. J. Luhmann (2014)
Cereb Cortex
   Abstract »    Full Text »    PDF »
Synaptic Input Correlations Leading to Membrane Potential Decorrelation of Spontaneous Activity in Cortex.
M. Graupner and A. D. Reyes (2013)
J. Neurosci. 33, 15075-15085
   Abstract »    Full Text »    PDF »
A new nonscanning confocal microscopy module for functional voltage-sensitive dye and Ca2+ imaging of neuronal circuit activity.
T. Tominaga and Y. Tominaga (2013)
J Neurophysiol 110, 553-561
   Abstract »    Full Text »    PDF »
Method for stationarity-segmentation of spike train data with application to the Pearson cross-correlation.
C. S. Quiroga-Lombard, J. Hass, and D. Durstewitz (2013)
J Neurophysiol 110, 562-572
   Abstract »    Full Text »    PDF »
Protracted Postnatal Development of Sparse, Specific Dentate Granule Cell Activation in the Mouse Hippocampus.
E. P. Yu, C. G. Dengler, S. F. Frausto, M. E. Putt, C. Yue, H. Takano, and D. A. Coulter (2013)
J. Neurosci. 33, 2947-2960
   Abstract »    Full Text »    PDF »
Interpyramid Spike Transmission Stabilizes the Sparseness of Recurrent Network Activity.
Y. Ikegaya, T. Sasaki, D. Ishikawa, N. Honma, K. Tao, N. Takahashi, G. Minamisawa, S. Ujita, and N. Matsuki (2013)
Cereb Cortex 23, 293-304
   Abstract »    Full Text »    PDF »
Layer III Neurons Control Synchronized Waves in the Immature Cerebral Cortex.
S. Namiki, H. Norimoto, C. Kobayashi, K. Nakatani, N. Matsuki, and Y. Ikegaya (2013)
J. Neurosci. 33, 987-1001
   Abstract »    Full Text »    PDF »
Fluoxetine (Prozac) and Serotonin Act on Excitatory Synaptic Transmission to Suppress Single Layer 2/3 Pyramidal Neuron-Triggered Cell Assemblies in the Human Prefrontal Cortex.
G. Komlosi, G. Molnar, M. Rozsa, S. Olah, P. Barzo, and G. Tamas (2012)
J. Neurosci. 32, 16369-16378
   Abstract »    Full Text »    PDF »
Schaffer-Specific Local Field Potentials Reflect Discrete Excitatory Events at Gamma Frequency That May Fire Postsynaptic Hippocampal CA1 Units.
A. Fernandez-Ruiz, V. A. Makarov, N. Benito, and O. Herreras (2012)
J. Neurosci. 32, 5165-5176
   Abstract »    Full Text »    PDF »
Deterministic and Stochastic Neuronal Contributions to Distinct Synchronous CA3 Network Bursts.
H. Takano, M. McCartney, P. I. Ortinski, C. Yue, M. E. Putt, and D. A. Coulter (2012)
J. Neurosci. 32, 4743-4754
   Abstract »    Full Text »    PDF »
A Candidate Mechanism Underlying the Variance of Interictal Spike Propagation.
H. R. Sabolek, W. B. Swiercz, K. P. Lillis, S. S. Cash, G. Huberfeld, G. Zhao, L. Ste. Marie, S. Clemenceau, G. Barsh, R. Miles, et al. (2012)
J. Neurosci. 32, 3009-3021
   Abstract »    Full Text »    PDF »
Locally Synchronized Synaptic Inputs.
N. Takahashi, K. Kitamura, N. Matsuo, M. Mayford, M. Kano, N. Matsuki, and Y. Ikegaya (2012)
Science 335, 353-356
   Abstract »    Full Text »    PDF »
Conditional modeling and the jitter method of spike resampling.
A. Amarasingham, M. T. Harrison, N. G. Hatsopoulos, and S. Geman (2012)
J Neurophysiol 107, 517-531
   Abstract »    Full Text »    PDF »
Slow and fast rhythms generated in the cerebral cortex of the anesthetized mouse.
M. Ruiz-Mejias, L. Ciria-Suarez, M. Mattia, and M. V. Sanchez-Vives (2011)
J Neurophysiol 106, 2910-2921
   Abstract »    Full Text »    PDF »
The Local Field Potential Reflects Surplus Spike Synchrony.
M. Denker, S. Roux, H. Linden, M. Diesmann, A. Riehle, and S. Grun (2011)
Cereb Cortex 21, 2681-2695
   Abstract »    Full Text »    PDF »
Emergence of Persistent Networks in Long-Term Intracranial EEG Recordings.
M. A. Kramer, U. T. Eden, K. Q. Lepage, E. D. Kolaczyk, M. T. Bianchi, and S. S. Cash (2011)
J. Neurosci. 31, 15757-15767
   Abstract »    Full Text »    PDF »
Dopaminergic Modulation of the Striatal Microcircuit: Receptor-Specific Configuration of Cell Assemblies.
L. Carrillo-Reid, S. Hernandez-Lopez, D. Tapia, E. Galarraga, and J. Bargas (2011)
J. Neurosci. 31, 14972-14983
   Abstract »    Full Text »    PDF »
Hippocampal Polysynaptic Computation.
R. Kimura, S. Kang, N. Takahashi, A. Usami, N. Matsuki, T. Fukai, and Y. Ikegaya (2011)
J. Neurosci. 31, 13168-13179
   Abstract »    Full Text »    PDF »
Locally Synchronized Astrocytes.
T. Sasaki, N. Kuga, S. Namiki, N. Matsuki, and Y. Ikegaya (2011)
Cereb Cortex 21, 1889-1900
   Abstract »    Full Text »    PDF »
Visual Experience-Dependent Maturation of Correlated Neuronal Activity Patterns in a Developing Visual System.
H. Xu, A. S. Khakhalin, A. V. Nurmikko, and C. D. Aizenman (2011)
J. Neurosci. 31, 8025-8036
   Abstract »    Full Text »    PDF »
A Subtraction Mechanism of Temporal Coding in Cerebellar Cortex.
B. E. Kalmbach, H. Voicu, T. Ohyama, and M. D. Mauk (2011)
J. Neurosci. 31, 2025-2034
   Abstract »    Full Text »    PDF »
Spike-Train Communities: Finding Groups of Similar Spike Trains.
M. D. Humphries (2011)
J. Neurosci. 31, 2321-2336
   Abstract »    Full Text »    PDF »
Fast Nonnegative Deconvolution for Spike Train Inference From Population Calcium Imaging.
J. T. Vogelstein, A. M. Packer, T. A. Machado, T. Sippy, B. Babadi, R. Yuste, and L. Paninski (2010)
J Neurophysiol 104, 3691-3704
   Abstract »    Full Text »    PDF »
Dynamics of the Parkinsonian Striatal Microcircuit: Entrainment into a Dominant Network State.
O. Jaidar, L. Carrillo-Reid, A. Hernandez, R. Drucker-Colin, J. Bargas, and A. Hernandez-Cruz (2010)
J. Neurosci. 30, 11326-11336
   Abstract »    Full Text »    PDF »
Precise Spatiotemporal Patterns among Visual Cortical Areas and Their Relation to Visual Stimulus Processing.
I. Ayzenshtat, E. Meirovithz, H. Edelman, U. Werner-Reiss, E. Bienenstock, M. Abeles, and H. Slovin (2010)
J. Neurosci. 30, 11232-11245
   Abstract »    Full Text »    PDF »
Circuit topology for synchronizing neurons in spontaneously active networks.
N. Takahashi, T. Sasaki, W. Matsumoto, N. Matsuki, and Y. Ikegaya (2010)
PNAS 107, 10244-10249
   Abstract »    Full Text »    PDF »
Sequentially Switching Cell Assemblies in Random Inhibitory Networks of Spiking Neurons in the Striatum.
A. Ponzi and J. Wickens (2010)
J. Neurosci. 30, 5894-5911
   Abstract »    Full Text »    PDF »
Reliable Recall of Spontaneous Activity Patterns in Cortical Networks.
O. Marre, P. Yger, A. P. Davison, and Y. Fregnac (2009)
J. Neurosci. 29, 14596-14606
   Abstract »    Full Text »    PDF »
Coordination of Rhythmic Motor Activity by Gradients of Synaptic Strength in a Neural Circuit That Couples Modular Neural Oscillators.
C. Smarandache, W. M. Hall, and B. Mulloney (2009)
J. Neurosci. 29, 9351-9360
   Abstract »    Full Text »    PDF »
Data-Driven Significance Estimation for Precise Spike Correlation.
S. Grun (2009)
J Neurophysiol 101, 1126-1140
   Abstract »    Full Text »    PDF »
Activation of the Cholinergic System Endows Compositional Properties to Striatal Cell Assemblies.
L. Carrillo-Reid, F. Tecuapetla, O. Ibanez-Sandoval, A. Hernandez-Cruz, E. Galarraga, and J. Bargas (2009)
J Neurophysiol 101, 737-749
   Abstract »    Full Text »    PDF »
Spatiotemporal Signatures of Large-Scale Synfire Chains for Speech Processing as Revealed by MEG.
F. Pulvermuller and Y. Shtyrov (2009)
Cereb Cortex 19, 79-88
   Abstract »    Full Text »    PDF »
Encoding by Response Duration in the Basal Ganglia.
N. Parush, D. Arkadir, A. Nevet, G. Morris, N. Tishby, I. Nelken, and H. Bergman (2008)
J Neurophysiol 100, 3244-3252
   Abstract »    Full Text »    PDF »
The Statistics of Repeating Patterns of Cortical Activity Can Be Reproduced by a Model Network of Stochastic Binary Neurons.
A. Roxin, V. Hakim, and N. Brunel (2008)
J. Neurosci. 28, 10734-10745
   Abstract »    Full Text »    PDF »
Detecting Synfire Chain Activity Using Massively Parallel Spike Train Recording.
S. Schrader, S. Grun, M. Diesmann, and G. L. Gerstein (2008)
J Neurophysiol 100, 2165-2176
   Abstract »    Full Text »    PDF »
Fast and Accurate Detection of Action Potentials From Somatic Calcium Fluctuations.
T. Sasaki, N. Takahashi, N. Matsuki, and Y. Ikegaya (2008)
J Neurophysiol 100, 1668-1676
   Abstract »    Full Text »    PDF »
GABA Neurons and the Mechanisms of Network Oscillations: Implications for Understanding Cortical Dysfunction in Schizophrenia.
G. Gonzalez-Burgos and D. A. Lewis (2008)
Schizophr Bull 34, 944-961
   Abstract »    Full Text »    PDF »
Nonperiodic Synchronization in Heterogeneous Networks of Spiking Neurons.
J.-P. Thivierge and P. Cisek (2008)
J. Neurosci. 28, 7968-7978
   Abstract »    Full Text »    PDF »
Topological analysis of population activity in visual cortex.
G. Singh, F. Memoli, T. Ishkhanov, G. Sapiro, G. Carlsson, and D. L. Ringach (2008)
J Vis 8, 11
   Abstract »    Full Text »    PDF »
D1-Like Dopamine Receptor Activation Modulates GABAergic Inhibition But Not Electrical Coupling between Neocortical Fast-Spiking Interneurons.
S. K. Towers and S. Hestrin (2008)
J. Neurosci. 28, 2633-2641
   Abstract »    Full Text »    PDF »
Visualizing Striatal Networks. Focus on: "Encoding Network States by Striatal Cell Assemblies".
S. Rayport (2008)
J Neurophysiol 99, 1053-1054
   Full Text »    PDF »
Encoding Network States by Striatal Cell Assemblies.
L. Carrillo-Reid, F. Tecuapetla, D. Tapia, A. Hernandez-Cruz, E. Galarraga, R. Drucker-Colin, and J. Bargas (2008)
J Neurophysiol 99, 1435-1450
   Abstract »    Full Text »    PDF »
Three-Dimensional Mapping of Unitary Synaptic Connections by Two-Photon Macro Photolysis of Caged Glutamate.
M. Matsuzaki, G. C. R. Ellis-Davies, and H. Kasai (2008)
J Neurophysiol 99, 1535-1544
   Abstract »    Full Text »    PDF »
A Maximum Entropy Model Applied to Spatial and Temporal Correlations from Cortical Networks In Vitro.
A. Tang, D. Jackson, J. Hobbs, W. Chen, J. L. Smith, H. Patel, A. Prieto, D. Petrusca, M. I. Grivich, A. Sher, et al. (2008)
J. Neurosci. 28, 505-518
   Abstract »    Full Text »    PDF »
Pathway-specific use-dependent dynamics of excitatory synaptic transmission in rat intracortical circuits.
S. R. Williams and S. E. Atkinson (2007)
J. Physiol. 585, 759-777
   Abstract »    Full Text »    PDF »
Spatial Organization of Neuronal Population Responses in Layer 2/3 of Rat Barrel Cortex.
J. N. D. Kerr, C. P. J. de Kock, D. S. Greenberg, R. M. Bruno, B. Sakmann, and F. Helmchen (2007)
J. Neurosci. 27, 13316-13328
   Abstract »    Full Text »    PDF »
Bioluminescent imaging of Ca2+ activity reveals spatiotemporal dynamics in glial networks of dark-adapted mouse retina.
C. Agulhon, J.-C. Platel, B. Kolomiets, V. Forster, S. Picaud, J. Brocard, P. Faure, and P. Brulet (2007)
J. Physiol. 583, 945-958
   Abstract »    Full Text »    PDF »
Neural Populations Can Induce Reliable Postsynaptic Currents without Observable Spike Rate Changes or Precise Spike Timing.
B. Tripp and C. Eliasmith (2007)
Cereb Cortex 17, 1830-1840
   Abstract »    Full Text »    PDF »
Temporal Integration by Stochastic Recurrent Network Dynamics With Bimodal Neurons.
H. Okamoto, Y. Isomura, M. Takada, and T. Fukai (2007)
J Neurophysiol 97, 3859-3867
   Abstract »    Full Text »    PDF »
Development and Plasticity of Spontaneous Activity and Up States in Cortical Organotypic Slices.
H. A. Johnson and D. V. Buonomano (2007)
J. Neurosci. 27, 5915-5925
   Abstract »    Full Text »    PDF »
Dynamical Basis of Irregular Spiking in NMDA-Driven Prefrontal Cortex Neurons.
D. Durstewitz and T. Gabriel (2007)
Cereb Cortex 17, 894-908
   Abstract »    Full Text »    PDF »
Feedforward Inhibition Contributes to the Control of Epileptiform Propagation Speed.
A. J. Trevelyan, D. Sussillo, and R. Yuste (2007)
J. Neurosci. 27, 3383-3387
   Abstract »    Full Text »    PDF »
Metastability of Active CA3 Networks.
T. Sasaki, N. Matsuki, and Y. Ikegaya (2007)
J. Neurosci. 27, 517-528
   Abstract »    Full Text »    PDF »
Sequential structure of neocortical spontaneous activity in vivo.
A. Luczak, P. Bartho, S. L. Marguet, G. Buzsaki, and K. D. Harris (2007)
PNAS 104, 347-352
   Abstract »    Full Text »    PDF »
Correlation Between Axonal Morphologies and Synaptic Input Kinetics of Interneurons from Mouse Visual Cortex.
D. Dumitriu, R. Cossart, J. Huang, and R. Yuste (2007)
Cereb Cortex 17, 81-91
   Abstract »    Full Text »    PDF »
Modular Propagation of Epileptiform Activity: Evidence for an Inhibitory Veto in Neocortex.
A. J. Trevelyan, D. Sussillo, B. O. Watson, and R. Yuste (2006)
J. Neurosci. 26, 12447-12455
   Abstract »    Full Text »    PDF »
Non-Gaussian Membrane Potential Dynamics Imply Sparse, Synchronous Activity in Auditory Cortex..
M. R. DeWeese and A. M. Zador (2006)
J. Neurosci. 26, 12206-12218
   Abstract »    Full Text »    PDF »
Glomerulus-specific, long-latency activity in the olfactory bulb granule cell network..
V. Kapoor and N. N. Urban (2006)
J. Neurosci. 26, 11709-11719
   Abstract »    Full Text »    PDF »
Dynamics and Effective Topology Underlying Synchronization in Networks of Cortical Neurons..
D. Eytan and S. Marom (2006)
J. Neurosci. 26, 8465-8476
   Abstract »    Full Text »    PDF »
Inverted-U Profile of Dopamine-NMDA-Mediated Spontaneous Avalanche Recurrence in Superficial Layers of Rat Prefrontal Cortex.
C. V. Stewart and D. Plenz (2006)
J. Neurosci. 26, 8148-8159
   Abstract »    Full Text »    PDF »
Integrative spike dynamics of rat CA1 neurons: a multineuronal imaging study.
T. Sasaki, R. Kimura, M. Tsukamoto, N. Matsuki, and Y. Ikegaya (2006)
J. Physiol. 574, 195-208
   Abstract »    Full Text »    PDF »
Extending the effects of spike-timing-dependent plasticity to behavioral timescales.
P. J. Drew and L. F. Abbott (2006)
PNAS 103, 8876-8881
   Abstract »    Full Text »    PDF »
Single Neurons Can Induce Phase Transitions of Cortical Recurrent Networks with Multiple Internal States.
S. Fujisawa, N. Matsuki, and Y. Ikegaya (2006)
Cereb Cortex 16, 639-654
   Abstract »    Full Text »    PDF »
Excitatory Effect of GABAergic Axo-Axonic Cells in Cortical Microcircuits.
J. Szabadics, C. Varga, G. Molnar, S. Olah, P. Barzo, and G. Tamas (2006)
Science 311, 233-235
   Abstract »    Full Text »    PDF »
Fast Functional Imaging of Single Neurons Using Random-Access Multiphoton (RAMP) Microscopy.
V. Iyer, T. M. Hoogland, and P. Saggau (2006)
J Neurophysiol 95, 535-545
   Abstract »    Full Text »    PDF »
Imaging input and output dynamics of neocortical networks in vivo: Exciting times ahead.
A. Grinvald (2005)
PNAS 102, 14125-14126
   Full Text »    PDF »
A Learning Rule for the Emergence of Stable Dynamics and Timing in Recurrent Networks.
D. V. Buonomano (2005)
J Neurophysiol 94, 2275-2283
   Abstract »    Full Text »    PDF »
From The Cover: Imaging input and output of neocortical networks in vivo.
J. N. D. Kerr, D. Greenberg, and F. Helmchen (2005)
PNAS 102, 14063-14068
   Abstract »    Full Text »    PDF »
Widely Distributed Magnetoencephalography Spikes Related to the Planning and Execution of Human Saccades.
A. A. Ioannides, P. B. C. Fenwick, and L. Liu (2005)
J. Neurosci. 25, 7950-7967
   Abstract »    Full Text »    PDF »
Spike Timing in CA3 Pyramidal Cells During Behavior: Implications for Synaptic Transmission.
M. Frerking, J. Schulte, S. P. Wiebe, and U. Staubli (2005)
J Neurophysiol 94, 1528-1540
   Abstract »    Full Text »    PDF »
Synaptic mechanisms of persistent reverberatory activity in neuronal networks.
P.-M. Lau and G.-Q. Bi (2005)
PNAS 102, 10333-10338
   Abstract »    Full Text »    PDF »
Synchronous neural activity in scale-free network models versus random network models.
G. Grinstein and R. Linsker (2005)
PNAS 102, 9948-9953
   Abstract »    Full Text »    PDF »
Encoding and Decoding of Dendritic Excitation during Active States in Pyramidal Neurons.
S. R. Williams (2005)
J. Neurosci. 25, 5894-5902
   Abstract »    Full Text »    PDF »
A Combinatorial Method for Analyzing Sequential Firing Patterns Involving an Arbitrary Number of Neurons Based on Relative Time Order.
A. K. Lee and M. A. Wilson (2004)
J Neurophysiol 92, 2555-2573
   Abstract »    Full Text »    PDF »
NEUROSCIENCE: Enhanced: Time Is Precious.
M. Abeles (2004)
Science 304, 523-524
   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