 |
Previous Article | Next Article 
The Journal of Neuroscience, November 1, 1999, 19(21):9497-9507
Replay and Time Compression of Recurring Spike Sequences in the
Hippocampus
Zoltán
Nádasdy,
Hajime
Hirase,
András
Czurkó,
Jozsef
Csicsvari, and
György
Buzsáki
Center for Molecular and Behavioral Neuroscience, Rutgers, The
State University of New Jersey, Newark, New Jersey
07102
Information in neuronal networks may be represented by the
spatiotemporal patterns of spikes. Here we examined the temporal coordination of pyramidal cell spikes in the rat hippocampus during slow-wave sleep. In addition, rats were trained to run in a defined position in space (running wheel) to activate a selected group of
pyramidal cells. A template-matching method and a joint probability map
method were used for sequence search. Repeating spike sequences in
excess of chance occurrence were examined by comparing the number of
repeating sequences in the original spike trains and in surrogate
trains after Monte Carlo shuffling of the spikes. Four different
shuffling procedures were used to control for the population dynamics
of hippocampal neurons. Repeating spike sequences in the recorded cell
assemblies were present in both the awake and sleeping animal in excess
of what might be predicted by random variations. Spike sequences
observed during wheel running were "replayed" at a faster timescale
during single sharp-wave bursts of slow-wave sleep. We hypothesize that
the endogenously expressed spike sequences during sleep reflect
reactivation of the circuitry modified by previous experience.
Reactivation of acquired sequences may serve to consolidate information.
Key words:
sharp waves; ; memory; coding; decoding; retrieval; network; sleep
Copyright © 1999 Society for Neuroscience 0270-6474/99/19219497-11$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
S. Gais, B. Rasch, U. Wagner, and J. Born
Visual-Procedural Memory Consolidation during Sleep Blocked by Glutamatergic Receptor Antagonists
J. Neurosci.,
May 21, 2008;
28(21):
5513 - 5518.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
O. Eschenko, W. Ramadan, M. Molle, J. Born, and S. J. Sara
Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning
Learn. Mem.,
April 2, 2008;
15(4):
222 - 228.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. R. Euston, M. Tatsuno, and B. L. McNaughton
Fast-Forward Playback of Recent Memory Sequences in Prefrontal Cortex During Sleep
Science,
November 16, 2007;
318(5853):
1147 - 1150.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Johnson and A. D. Redish
Neural Ensembles in CA3 Transiently Encode Paths Forward of the Animal at a Decision Point
J. Neurosci.,
November 7, 2007;
27(45):
12176 - 12189.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Clemens, M. Molle, L. Eross, P. Barsi, P. Halasz, and J. Born
Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans
Brain,
November 1, 2007;
130(11):
2868 - 2878.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. D. REDISH and A. JOHNSON
A Computational Model of Craving and Obsession
Ann. N.Y. Acad. Sci.,
May 1, 2007;
1104(1):
324 - 339.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. T. G. Hahn, B. Sakmann, and M. R. Mehta
Differential responses of hippocampal subfields to cortical up-down states
PNAS,
March 20, 2007;
104(12):
5169 - 5174.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Chi, W. Wu, Z. Haga, N. G. Hatsopoulos, and D. Margoliash
Template-Based Spike Pattern Identification With Linear Convolution and Dynamic Time Warping
J Neurophysiol,
February 1, 2007;
97(2):
1221 - 1235.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. H. R. Hahnloser and M. S. Fee
Sleep-Related Spike Bursts in HVC Are Driven by the Nucleus Interface of the Nidopallium
J Neurophysiol,
January 1, 2007;
97(1):
423 - 435.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. C. Jackson, A. Johnson, and A. D. Redish
Hippocampal Sharp Waves and Reactivation during Awake States Depend on Repeated Sequential Experience
J. Neurosci.,
November 29, 2006;
26(48):
12415 - 12426.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Shmiel, R. Drori, O. Shmiel, Y. Ben-Shaul, Z. Nadasdy, M. Shemesh, M. Teicher, and M. Abeles
Temporally Precise Cortical Firing Patterns Are Associated With Distinct Action Segments
J Neurophysiol,
November 1, 2006;
96(5):
2645 - 2652.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Tatsuno, P. Lipa, and B. L. McNaughton
Methodological considerations on the use of template matching to study long-lasting memory trace replay.
J. Neurosci.,
October 18, 2006;
26(42):
10727 - 10742.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. H. R. Hahnloser, A. A. Kozhevnikov, and M. S. Fee
Sleep-Related Neural Activity in a Premotor and a Basal-Ganglia Pathway of the Songbird
J Neurophysiol,
August 1, 2006;
96(2):
794 - 812.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. J. Drew and L. F. Abbott
Extending the effects of spike-timing-dependent plasticity to behavioral timescales
PNAS,
June 6, 2006;
103(23):
8876 - 8881.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. C. Smith and P. Smith
A set probability technique for detecting relative time order across multiple neurons.
Neural Comput.,
May 1, 2006;
18(5):
1197 - 1214.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Leibold and R. Kempter
Memory capacity for sequences in a recurrent network with biological constraints.
Neural Comput.,
April 1, 2006;
18(4):
904 - 941.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Tino and A. J. S. Mills
Learning beyond finite memory in recurrent networks of spiking neurons.
Neural Comput.,
March 1, 2006;
18(3):
591 - 613.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Gasparini and J. C. Magee
State-Dependent Dendritic Computation in Hippocampal CA1 Pyramidal Neurons
J. Neurosci.,
February 15, 2006;
26(7):
2088 - 2100.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. M. McDermott, M. N. Hardy, N. G. Bazan, and J. C. Magee
Sleep deprivation-induced alterations in excitatory synaptic transmission in the CA1 region of the rat hippocampus
J. Physiol.,
February 1, 2006;
570(3):
553 - 565.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Takashima, K. M. Petersson, F. Rutters, I. Tendolkar, O. Jensen, M. J. Zwarts, B. L. McNaughton, and G. Fernandez
From the Cover: Declarative memory consolidation in humans: A prospective functional magnetic resonance imaging study
PNAS,
January 17, 2006;
103(3):
756 - 761.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Shmiel, R. Drori, O. Shmiel, Y. Ben-Shaul, Z. Nadasdy, M. Shemesh, M. Teicher, and M. Abeles
Neurons of the cerebral cortex exhibit precise interspike timing in correspondence to behavior
PNAS,
December 20, 2005;
102(51):
18655 - 18657.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. K. Jha, B. E. Jones, T. Coleman, N. Steinmetz, C.-T. Law, G. Griffin, J. Hawk, N. Dabbish, V. A. Kalatsky, and M. G. Frank
Sleep-Dependent Plasticity Requires Cortical Activity
J. Neurosci.,
October 5, 2005;
25(40):
9266 - 9274.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Grinstein and R. Linsker
Synchronous neural activity in scale-free network models versus random network models
PNAS,
July 12, 2005;
102(28):
9948 - 9953.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. G. Pelletier, E. Likhtik, M. Filali, and D. Pare
Lasting increases in basolateral amygdala activity after emotional arousal: Implications for facilitated consolidation of emotional memories
Learn. Mem.,
March 1, 2005;
12(2):
96 - 102.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. V. Samsonovich and G. A. Ascoli
A simple neural network model of the hippocampus suggesting its pathfinding role in episodic memory retrieval
Learn. Mem.,
March 1, 2005;
12(2):
193 - 208.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Marshall, M. Molle, M. Hallschmid, and J. Born
Transcranial Direct Current Stimulation during Sleep Improves Declarative Memory
J. Neurosci.,
November 3, 2004;
24(44):
9985 - 9992.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Ribeiro and M. A.L. Nicolelis
Reverberation, storage, and postsynaptic propagation of memories during sleep
Learn. Mem.,
November 1, 2004;
11(6):
686 - 696.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. K. Lee and M. A. Wilson
A Combinatorial Method for Analyzing Sequential Firing Patterns Involving an Arbitrary Number of Neurons Based on Relative Time Order
J Neurophysiol,
October 1, 2004;
92(4):
2555 - 2573.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Molle, L. Marshall, S. Gais, and J. Born
Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations
PNAS,
September 21, 2004;
101(38):
13963 - 13968.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. M. Beggs and D. Plenz
Neuronal Avalanches Are Diverse and Precise Activity Patterns That Are Stable for Many Hours in Cortical Slice Cultures
J. Neurosci.,
June 2, 2004;
24(22):
5216 - 5229.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Jarosiewicz and W. E. Skaggs
Level of Arousal During the Small Irregular Activity State in the Rat Hippocampal EEG
J Neurophysiol,
June 1, 2004;
91(6):
2649 - 2657.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. G. Pelletier, J. Apergis, and D. Pare
Low-Probability Transmission of Neocortical and Entorhinal Impulses Through the Perirhinal Cortex
J Neurophysiol,
May 1, 2004;
91(5):
2079 - 2089.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Ikegaya, G. Aaron, R. Cossart, D. Aronov, I. Lampl, D. Ferster, and R. Yuste
Synfire Chains and Cortical Songs: Temporal Modules of Cortical Activity
Science,
April 23, 2004;
304(5670):
559 - 564.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. Szita and A. Lorincz
Kalman Filter Control Embedded into the Reinforcement Learning Framework
Neural Comput.,
March 1, 2004;
16(3):
491 - 499.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Gais and J. Born
From The Cover: Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation
PNAS,
February 17, 2004;
101(7):
2140 - 2144.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Chi, P. L. Rauske, and D. Margoliash
Pattern Filtering for Detection of Neural Activity, with Examples from HVc Activity During Sleep in Zebra Finches
Neural Comput.,
October 1, 2003;
15(10):
2307 - 2337.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. DESTEXHE and T. J. SEJNOWSKI
Interactions Between Membrane Conductances Underlying Thalamocortical Slow-Wave Oscillations
Physiol Rev,
October 1, 2003;
83(4):
1401 - 1453.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. E. Hampson, S.-y. Zhuang, J. L. Weiner, and S. A. Deadwyler
Functional Significance of Cannabinoid-Mediated, Depolarization-Induced Suppression of Inhibition (DSI) in the Hippocampus
J Neurophysiol,
July 1, 2003;
90(1):
55 - 64.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Degenetais, A.-M. Thierry, J. Glowinski, and Y. Gioanni
Synaptic Influence of Hippocampus on Pyramidal Cells of the Rat Prefrontal Cortex: An In Vivo Intracellular Recording Study
Cereb Cortex,
July 1, 2003;
13(7):
782 - 792.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Maquet, S. Schwartz, R. Passingham, and C. Frith
Sleep-Related Consolidation of a Visuomotor Skill: Brain Mechanisms as Assessed by Functional Magnetic Resonance Imaging
J. Neurosci.,
February 15, 2003;
23(4):
1432 - 1440.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Nakahara and S.-i. Amari
Information-Geometric Measure for Neural Spikes
Neural Comput.,
October 1, 2002;
14(10):
2269 - 2316.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
K. L. Hoffman and B. L. McNaughton
Coordinated Reactivation of Distributed Memory Traces in Primate Neocortex
Science,
September 20, 2002;
297(5589):
2070 - 2073.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Gais, M. Molle, K. Helms, and J. Born
Learning-Dependent Increases in Sleep Spindle Density
J. Neurosci.,
August 1, 2002;
22(15):
6830 - 6834.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Grun, M. Diesmann, and A. Aertsen
Unitary Events in Multiple Single-Neuron Spiking Activity: I. Detection and Significance
Neural Comput.,
January 1, 2002;
14(1):
43 - 80.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Maquet
The Role of Sleep in Learning and Memory
Science,
November 2, 2001;
294(5544):
1048 - 1052.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Grenier, I. Timofeev, and M. Steriade
Focal Synchronization of Ripples (80-200 Hz) in Neocortex and Their Neuronal Correlates
J Neurophysiol,
October 1, 2001;
86(4):
1884 - 1898.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. A. Gusev and D. L. Alkon
Intracellular Correlates of Spatial Memory Acquisition in Hippocampal Slices: Long-Term Disinhibition of CA1 Pyramidal Cells
J Neurophysiol,
August 1, 2001;
86(2):
881 - 899.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Hirase, X. Leinekugel, A. Czurko, J. Csicsvari, and G. Buzsaki
Firing rates of hippocampal neurons are preserved during subsequent sleep episodes and modified by novel awake experience
PNAS,
July 19, 2001;
(2001)
161274398.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. S. Dave and D. Margoliash
Song Replay During Sleep and Computational Rules for Sensorimotor Vocal Learning
Science,
October 27, 2000;
290(5492):
812 - 816.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
K. D. Harris, D. A. Henze, J. Csicsvari, H. Hirase, and G. Buzsaki
Accuracy of Tetrode Spike Separation as Determined by Simultaneous Intracellular and Extracellular Measurements
J Neurophysiol,
July 1, 2000;
84(1):
401 - 414.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. LORINCZ and G. BUZSAKI
Two-Phase Computational Model Training Long-Term Memories in the Entorhinal-Hippocampal Region
Ann. N.Y. Acad. Sci.,
June 1, 2000;
911(1):
83 - 111.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Hirase, X. Leinekugel, A. Czurko, J. Csicsvari, and G. Buzsaki
Firing rates of hippocampal neurons are preserved during subsequent sleep episodes and modified by novel awake experience
PNAS,
July 31, 2001;
98(16):
9386 - 9390.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Hirase, X. Leinekugel, J. Csicsvari, A. Czurko, and G. Buzsaki
Behavior-Dependent States of the Hippocampal Network Affect Functional Clustering of Neurons
J. Neurosci.,
May 15, 2001;
21(10):
RC145 - RC145.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|